an update on the novel genera and species and revised ... · february 2019 volume 57 issue 2...
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An Update on the Novel Genera and Species and RevisedTaxonomic Status of Bacterial Organisms Described in 2016and 2017
Erik Munson,a Karen C. Carrollb
aCollege of Health Sciences, Marquette University, Milwaukee, Wisconsin, USAbDivision of Medical Microbiology, Department of Pathology, The Johns Hopkins University School of Medicine, Baltimore, Maryland, USA
ABSTRACT Recognition and acknowledgment of novel bacterial taxonomy and no-menclature revisions can impact clinical practice, disease epidemiology, and routineclinical microbiology laboratory operations. The Journal of Clinical Microbiology (JCM)herein presents its biannual report summarizing such changes published in the years2016 and 2017, as published and added by the International Journal of Systematicand Evolutionary Microbiology. Noteworthy discussion centers around descriptions ofnovel Corynebacteriaceae and an anaerobic mycolic acid-producing bacterium in thesuborder Corynebacterineae; revisions within the Propionibacterium, Clostridium, Bor-relia, and Enterobacter genera; and a major reorganization of the family Enterobacte-riaceae. JCM intends to sustain this series of reports as advancements in moleculargenetics, whole-genome sequencing, and studies of the human microbiome con-tinue to produce novel taxa and clearer understandings of bacterial relatedness.
KEYWORDS bacteria, nomenclature, phylogenetics, taxonomy
In 2017, the Journal of Clinical Microbiology (JCM) published its first series of minire-views summarizing newly published novel microbial taxa and revisions to taxonomic
nomenclature within the disciplines of bacteriology (1), parasitology (2), virology (3),mycology (4), and mycobacteriology (5). With respect to bacteriology, this itemizationand discussion of novel taxa and changes to taxonomy are particularly relevant becausethese are often the by-products of human microbiome investigations and/or advance-ments in molecular genetics and genomic sequencing strategies. Applications oftaxonomic changes can be broad ranging. The impact on clinical care includes appro-priate utilization of antimicrobial susceptibility testing standards in terms of testprocurement and data interpretation (6) and a broader understanding of the patho-genesis and epidemiology of emerging pathogens (7, 8). In addition, nomenclaturechanges can directly impact a given clinical microbiology laboratory from an adminis-trative standpoint (conformity to accreditation checklist standards [9]). In a recentsurvey on the impact of taxonomic changes on clinical care sent to the AmericanSociety for Microbiology ClinMicroNet listserv, several respondents mentioned thechallenge of trying to know when changes are made and how to efficiently implementand communicate their relevance to both the laboratory and clinicians (K. Carroll,unpublished data).
As such, we add to the comprehensive capstone previously established (1, 10) byproviding a (second) biannual update of novel prokaryotic taxa and bacterial nomen-clature revisions published in the years 2016 and 2017. Unless otherwise indicated, thepresented organisms were derived from human clinical material and nomenclaturedesignations have been published or added by the International Journal of Systematicand Evolutionary Microbiology (IJSEM).
Citation Munson E, Carroll KC. 2019. An updateon the novel genera and species and revisedtaxonomic status of bacterial organismsdescribed in 2016 and 2017. J Clin Microbiol57:e01181-18. https://doi.org/10.1128/JCM.01181-18.
Editor Colleen Suzanne Kraft, Emory University
Copyright © 2019 American Society forMicrobiology. All Rights Reserved.
Address correspondence to Karen C. Carroll,[email protected].
Accepted manuscript posted online 26September 2018Published
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METHODSValidly published novel and revised taxa pertinent to prokaryotic species must meet
one of two requirements: (i) they must be described in an original investigationpublished in IJSEM, or (ii) they must be described in a study published in an alternativejournal with later inclusion on an approved list in IJSEM. Journals that have publishedstudies providing an effective description of validly named new taxa which may berelevant to the practice of clinical microbiology include Anaerobe; Antonie Van Leeu-wenhoek; APMIS; Clinical Microbiology and Infection; Current Microbiology; DiagnosticMicrobiology and Infectious Disease; Emerging Microbes and Infections; Frontiers in Ge-netics; Frontiers in Microbiology; Infection, Genetics and Evolution; Journal of AntimicrobialChemotherapy; JCM; Journal of General and Applied Microbiology; Microbiology andImmunology; Microbiologyopen; New Microbes and New Infections; Research in Microbi-ology; Standards in Genomic Sciences; and Systematic and Applied Microbiology. Six timesper year, IJSEM publishes papers entitled “List of new names and new combinationspreviously effectively, but not validly, published” (an example is provided in reference11). To be considered for inclusion on this approved list, authors must submit a copyof the published article to the editorial office of IJSEM for confirmation that all elementsnecessary for valid publication have been met. In addition, type strains are to bedeposited into recognized culture collections in two separate countries. Taxa on theseapproved lists may be subject to reclassification on the basis of a synonym designationor transfer to another genus. Within this article, taxa that were previously and effec-tively described in journals outside of IJSEM are footnoted in such fashion.
All issues of IJSEM published from January 2016 through December 2017 weresearched for original articles describing new species taxonomy or accepted changes intaxonomic nomenclature. This audit was further filtered by organisms recovered fromhuman sources. When an initial organism reservoir could not be ascertained, PubMedprimary literature searches (U.S. National Library of Medicine and the National Institutesof Health) of the novel or revised taxon attempted to index subsequent case reports forfurther investigation; several of these case reports are referenced throughout thisarticle. A number of IJSEM publications simply identified isolates as being derived froma specific specimen source (including sterile body sites) but did not provide contextualclinical data. Therefore, in these scenarios (including for a number of novel taxa derivedfrom blood culture), the clinical significance of these taxa was interpreted as “notestablished” (examples are provided in references 12 to 21). (By way of PubMed primaryliterature searches, attempts were also made to investigate the uncertain clinicalsignificance of previously reported novel and revised taxa [1]). Additional studies maybe necessary to characterize the ultimate clinical significance of novel taxa (22).
Twice per year, IJSEM publishes papers entitled “Notification of changes in taxo-nomic opinion previously published outside the IJSEM.” The journal publicizes thesechanges in taxonomic opinion simply as a service to bacteriology, rather than state-ments of validly published or approved taxonomy. No such reports pertaining toisolates derived from human sources were found in searches of IJSEM literature from2016 and 2017; two such publications from 2014 and 2015 (23, 24) were noted in theprevious minireview (1). Future JCM taxonomy compendia will report pertinent findingsfrom such publications in an effort to subsequently ascertain either the true clinicalsignificance of isolates or determine if official taxonomic status has been granted.
RESULTS AND DISCUSSION
Table 1 is a compilation of novel taxa recovered from human sources stratified byGram reaction, cellular morphology, and oxygen requirement for growth. Table 2 liststaxonomic revisions for organisms recovered from human sources. Finally, Table 3, onthe basis of recent peer-reviewed publications, attempts to retrospectively ascribeclinical significance to a number of organisms whose clinical significance was notestablished in the previous taxonomy compendium or to add new knowledge fororganisms recovered from clinical infections (1). Those findings warranting emphasisare discussed below.
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TAB
LE1
New
bac
teria
lsp
ecie
sre
cove
red
from
hum
ancl
inic
alm
ater
ial
rep
orte
dfr
omJa
nuar
y20
16th
roug
hD
ecem
ber
2017
Scie
nti
ficn
ame
Fam
ilySo
urce
Clin
ical
rele
van
ceG
row
thch
arac
teri
stic
sRe
fere
nce
(s)
Gra
m-p
ositi
veco
cci
Stre
ptoc
occu
sha
licho
eri
sub
sp.
hom
inis
sub
sp.n
ov.
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ptoc
occa
ceae
Bloo
d,em
pye
ma,
sinu
sA
tle
ast
one
pat
ient
had
sep
sis
Gra
m-p
ositi
veco
cci
occu
rrin
gin
pai
rsor
chai
ns;n
on-s
por
efo
rmin
g;hy
drol
yzes
bile
escu
lin;
colo
nyde
scrip
tion
issi
mila
rto
the
spec
ies
desc
riptio
np
rovi
ded
inre
fere
nce
25;c
olon
ies
are
whi
te,n
onhe
mol
ytic
,and
umb
onat
e;La
ncefi
eld
grou
pB
25–2
7
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icoc
cus
indi
cus
gen.
nov.
,sp
.nov
.St
aphy
loco
ccac
eae
Skin
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ated
from
the
exte
rnal
ear
ofa
heal
thy
hum
anG
ram
-pos
itive
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bic
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i,no
nmot
ile,n
on-s
por
efo
rmin
g;p
ositi
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tala
sean
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idas
e;gr
ows
bet
wee
n20
and
40°C
,with
optim
umgr
owth
at35
°C28
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m-p
ositi
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acill
iTs
ukam
urel
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ngko
ngen
sis
sp.n
ov.
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amur
ella
ceae
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neal
scra
pin
g;b
lood
cult
ure
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ated
from
ap
atie
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ratit
isan
da
seco
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atie
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ithca
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rem
ia;b
oth
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ient
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ere
from
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gKo
ng
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obic
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ositi
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otile
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ore-
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ing
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illus
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alas
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ositi
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row
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est
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with
5%de
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ated
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onie
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eor
ange
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dro
ugh
afte
r48
hof
incu
bat
ion
at37
°C
29
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amur
ella
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nsis
sp. n
ov.
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amur
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junc
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ated
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atie
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ctiv
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obic
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-sp
ore-
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itive
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ws
bes
ton
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umb
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ith5%
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rinat
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odag
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ies
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whi
te,d
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ndro
ugh
afte
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bat
ion
at37
°C
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mab
acte
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gina
lissp
. nov
.D
erm
abac
tera
ceae
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nal
fluid
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esta
blis
hed;
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ated
from
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nal
fluid
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anfe
mal
e
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ltat
ive
anae
rob
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ram
-pos
itive
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rtb
acill
us;n
on-s
por
efo
rmin
g,no
nmot
ile,c
atal
ase
pos
itive
,oxi
dase
nega
tive;
crea
my
whi
teco
loni
esth
atgr
owop
timal
lyat
37°C
30
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mab
acte
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juen
sis
sp. n
ov.
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mab
acte
race
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sfr
oma
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ound
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ger
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lsar
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itive
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rm-li
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egr
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at30
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ells
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ition
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lera
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idas
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ositi
ve;
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isp
rodu
ced
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riety
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rboh
ydra
tes
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cter
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iisp
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.Co
ryne
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eria
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ocia
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with
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arin
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ions
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tto
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ium
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thG
ram
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itive
bac
illi
that
occu
rsi
ngly
orin
pal
isad
es,p
airs
,or
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apes
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onie
sar
esl
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owin
g(7
2h)
,con
vex
smoo
thgr
ay-w
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eige
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olyt
ic;g
row
sin
air,
in5%
CO
2,a
ndun
der
anae
rob
icco
nditi
ons
at37
°Cor
42°C
but
not
at25
°C;c
atal
ase
pos
itive
,oxi
dase
nega
tive,
nonm
otile
,lip
ophi
lic,u
reas
ep
ositi
ve,n
itrat
ene
gativ
e
32
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neba
cter
ium
ocul
isp
. nov
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ryne
bact
eria
ceae
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Ass
ocia
ted
with
ocul
arin
fect
ions
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tto
med
ium
-leng
thG
ram
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itive
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illi
that
occu
rsi
ngly
orin
pal
isad
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airs
,or
Vsh
apes
;col
onie
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esl
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owin
g(7
2h)
,con
vex
smoo
thgr
ay-w
hite
orlig
htb
eige
,no
nhem
olyt
ic;g
row
sin
air,
in5%
CO
2,a
ndun
der
anae
rob
icco
nditi
ons
at37
°Can
d42
°Cb
utno
tat
25°C
;cat
alas
ep
ositi
ve,o
xida
sene
gativ
e,no
nmot
ile,l
ipop
hilic
,ure
ase
pos
itive
,nitr
ate
nega
tive
32
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sone
llacl
evel
ande
nsis
gen.
nov.
, sp
.nov
.Su
bor
der
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neba
cter
inea
e;no
fam
ilyas
sign
men
t
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sces
ses
Ass
ocia
ted
with
ava
riety
ofhu
man
absc
esse
sin
the
bre
ast,
liver
,sp
ine,
per
itone
um
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mor
phi
cG
ram
-pos
itive
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ian
db
acill
i;p
artia
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idfa
st;f
orm
sp
inp
oint
,wax
yco
loni
eson
CD
Can
aero
bic
blo
odag
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ter
5–7
days
ofin
cub
atio
n;op
timal
grow
that
35°C
inan
envi
ronm
ent
of�
1.0%
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en
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5
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ardi
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inan
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sis
sp.
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ardi
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omth
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ueou
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mor
from
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atie
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htha
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s
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obic
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m-p
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otile
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ms
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eliu
m;g
row
sat
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d45
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ngen
sis
sp.
nov.
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ardi
acea
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ood
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vere
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omtw
op
atie
nts:
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efr
oma
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odcu
ltur
ean
din
the
othe
rfr
omp
erito
neal
dial
ysis
efflu
ent
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m-p
ositi
vem
odifi
edac
id-f
ast,
nons
por
ulat
ing
bac
illi;
grow
son
Col
umb
iaag
arw
ith5%
defib
rinat
edsh
eep
blo
odae
rob
ical
lyas
pin
kto
oran
geno
nhem
olyt
icco
loni
es;c
atal
ase
pos
itive
;oxi
dase
nega
tive
12
Cory
neba
cter
ium
gott
inge
nse
sp. n
ov.
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neba
cter
iace
aeBl
ood
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ated
from
the
blo
odof
ap
atie
ntw
ithb
acte
rem
iaof
unkn
own
orig
inin
Göt
tinge
n,G
erm
any
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m-p
ositi
ve,b
acill
us-s
hap
edb
acte
riath
atsh
owty
pic
alp
alis
ade
arra
ngem
ents
ofth
ece
lls;n
on-s
por
efo
rmin
g,ca
tala
sep
ositi
ve,o
xida
sene
gativ
e;fo
rms
whi
te-c
ream
circ
ular
colo
nies
onC
olum
bia
blo
odag
ar
13
Paen
ibac
illus
ihum
iisp
. nov
.Pa
enib
acill
acea
eaFe
ces
Not
esta
blis
hed;
the
isol
ate
was
from
afe
mal
ein
Fran
cep
rior
tob
aria
tric
surg
ery
Mot
ile,s
por
e-fo
rmin
g,G
ram
-pos
itive
bac
illus
(fre
quen
tly
over
deco
loriz
esin
Gra
mst
ain)
;op
timal
grow
that
37°C
;cap
able
ofgr
owth
unde
rm
icro
aero
phi
lican
dan
aero
bic
cond
ition
s;1-
to2-
mm
-dia
met
ergr
ayco
loni
eson
blo
od-e
nric
hed
Col
umb
iaag
ar;
cata
lase
and
urea
sene
gativ
e;ut
iliza
tion
ofse
vera
lca
rboh
ydra
tes
37b
Gra
m-n
egat
ive
cocc
iN
eiss
eria
dum
asia
nasp
.nov
.N
eiss
eria
ceae
Sput
um(n
�2)
Not
esta
blis
hed;
clin
ical
isol
ates
sub
mitt
edto
aU
.S.r
efer
ence
lab
orat
ory
in20
09an
d20
12
Facu
ltat
ive
anae
rob
ic,n
onm
otile
,oxi
dase
-pos
itive
Gra
m-n
egat
ive
cocc
usor
cocc
obac
illus
;op
timal
grow
that
37°C
;gra
y-p
igm
ente
d1.
9-to
2.8-
mm
-dia
met
erco
loni
escu
ltiv
ated
onch
ocol
ate
agar
pla
tes
sup
ple
men
ted
with
10%
hors
eb
lood
in5%
CO
2;c
atal
ase
and
pro
line
isom
eras
ep
ositi
ve;r
educ
esni
trat
eto
nitr
ite;a
cid
pro
duct
ion
from
D-g
luco
seb
utno
tfr
omm
alto
seor
sucr
ose
38
(Con
tinue
don
next
pag
e)
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TAB
LE1
(Con
tinue
d)
Scie
nti
ficn
ame
Fam
ilySo
urce
Clin
ical
rele
van
ceG
row
thch
arac
teri
stic
sRe
fere
nce
(s)
Gra
m-n
egat
ive
bac
illi
Ente
roba
cter
buga
nden
sis
sp.
nov.
Ente
roba
cter
iace
aeBl
ood
(17)
Isol
ates
from
ane
onat
alse
ptic
emia
outb
reak
inTa
nzan
ia;p
osse
ssed
the
CTX
-M
-15
resi
stan
cege
ne;r
esis
tant
toflu
oroq
uino
lone
,am
inog
lyco
side
,and
tetr
acyc
line
antim
icro
bia
ls
Col
onia
lgr
owth
cons
iste
ntw
ithth
atof
othe
rEn
tero
bact
ersp
p.;
lact
ose
ferm
enta
tion
obse
rved
only
afte
r24
hof
incu
bat
ion;
citr
ate,
argi
nine
dihy
drol
ase,
and
orni
thin
ede
carb
oxyl
ase
pos
itive
;lys
ine
deca
rbox
ylas
e,ur
ease
,and
Voge
s-Pr
oska
uer
nega
tive
39
Alk
anin
dige
sho
ngko
ngen
sis
sp.n
ov.
Mor
axel
lace
aePa
rotid
absc
ess
inci
sion
and
drai
nage
Infe
cted
War
thin
’stu
mor
resu
ltin
gin
par
otid
glan
dab
sces
san
dp
erip
hera
lle
ukoc
ytos
is;t
hep
atie
ntre
spon
ded
todr
aina
gean
dam
oxic
illin
-cla
vula
nate
Aer
obic
,non
mot
ile,o
xida
se-n
egat
ive
Gra
m-n
egat
ive
cocc
obac
illus
;0.5
-mm
-dia
met
er(n
onhe
mol
ytic
)co
loni
eson
blo
odan
dM
acC
onke
yag
ars
at37
°C;g
ener
alfa
ilure
tofe
rmen
tor
oxid
ize
carb
ohyd
rate
s
40c
Mic
rovi
rga
mas
silie
nsis
sp.n
ov.
Met
hylo
bact
eria
ceae
Fece
sN
otes
tab
lishe
d;p
osse
sses
the
larg
est
geno
me
(9.2
meg
abas
es)
ofan
yhu
man
isol
ate
Aer
obic
,non
mot
ile,n
on-s
por
e-fo
rmin
g,ox
idas
e-ne
gativ
eG
ram
-neg
ativ
eb
acill
us;c
olon
ies
pro
pag
ated
onm
odifi
ed7H
10m
ediu
msu
pp
lem
ente
dw
ithsh
eep
blo
od;o
ptim
algr
owth
at37
°C;l
euci
near
ylam
idas
e,ni
trat
ere
duct
ase,
and
cyst
eine
aryl
amid
ase
pos
itive
;alk
alin
ep
hosp
hata
sene
gativ
e
41d
Obl
itim
onas
alka
liphi
lage
n.no
v.,s
p.n
ovPs
eudo
mon
adac
eae
Urin
e(n
�3)
,leg
tissu
e(n
�2)
,liv
er,l
ung
tissu
e,an
dfo
otw
ound
spec
imen
s
Not
esta
blis
hed;
clin
ical
isol
ates
sub
mitt
edto
aU
.S.r
efer
ence
lab
orat
ory
from
1969
to19
79
Mic
roae
rop
hilic
,non
mot
ile,o
xida
se-p
ositi
veG
ram
-neg
ativ
eb
acill
us;g
row
thon
rout
ine
bac
terio
logi
cm
edia
(incl
udin
gb
lood
agar
and
Mac
Con
key
agar
);op
timal
grow
that
20–
35°C
;ure
a,ge
latin
,and
escu
linhy
drol
ysis
nega
tive;
leuc
ine
aryl
amid
ase
and
gluc
ose
oxid
atio
np
ositi
ve;l
acto
sean
dsu
cros
eut
iliza
tion
nega
tive
42
Burk
hold
eria
conc
itans
Burk
hold
eria
ceae
Lung
tissu
e,b
lood
Not
esta
blis
hed
Non
mot
ile,o
xida
se-p
ositi
veG
ram
-neg
ativ
eb
acill
us;l
ess
than
1-m
m-d
iam
eter
colo
nies
cult
ivat
edon
tryp
ticso
yan
dM
acC
onke
yag
ars
at15
–28°
C;p
ositi
vefo
rTw
een
60hy
drol
ysis
,neg
ativ
efo
rTw
een
80hy
drol
ysis
;ure
ase,
escu
linhy
drol
ysis
, �-g
alac
tosi
dase
,an
dca
pra
teas
sim
ilatio
nne
gativ
e;su
bse
quen
tta
xono
mic
revi
sion
desc
ribed
inTa
ble
2
14e
Burk
hold
eria
turb
ans
Burk
hold
eria
ceae
Pleu
ral
fluid
Not
esta
blis
hed
Non
mot
ile,o
xida
se-p
ositi
veG
ram
-neg
ativ
eb
acill
us;l
ess
than
1-m
m-d
iam
eter
colo
nies
cult
ivat
edon
tryp
ticso
yan
dM
acC
onke
yag
ars
at15
–37°
C;p
ositi
vefo
rTw
een
60hy
drol
ysis
,neg
ativ
efo
rTw
een
80hy
drol
ysis
;glu
cose
and
cap
rate
assi
mila
tion
pos
itive
;ur
ease
,esc
ulin
hydr
olys
is,a
nd�
-gal
acto
sida
sene
gativ
e;su
bse
quen
tta
xono
mic
revi
sion
isde
scrib
edin
Tab
le2
14e
Ach
rom
obac
ter
dele
yisp
.nov
.A
lcal
igen
eace
aePr
osta
ticse
cret
ion,
pha
ryng
eal
swab
Not
esta
blis
hed;
pha
ryng
eal
isol
ate
from
aU
.S.c
ystic
fibro
sis
pat
ient
Mot
ile,o
xida
se-p
ositi
veG
ram
-neg
ativ
eb
acill
us;n
onp
igm
ente
d1.
0-to
1.5-
mm
-dia
met
erco
loni
escu
ltiv
ated
ontr
yptic
soy
agar
at28
°C;g
row
thof
sele
cted
stra
ins
once
trim
ide
agar
inth
ep
rese
nce
of3.
0%an
d4.
5%N
aCl;
nitr
itere
duct
ion
and
deni
trifi
catio
nne
gativ
e;ca
pra
teas
sim
ilatio
nan
dal
kalin
ep
hosp
hata
sep
ositi
ve
43
Aci
neto
bact
erdi
jksh
oorn
iae
sp.
nov.
Mor
axel
lace
aeC
linic
alst
rain
s,in
clud
ing
thos
efr
omw
ound
(n�
3),
sput
um(n
�2)
,blo
od,
urin
e,ca
thet
er,a
ndne
phr
olog
ydr
ain
spec
imen
s
Not
esta
blis
hed
Aer
obic
,non
mot
ile,o
xida
se-n
egat
ive
Gra
m-n
egat
ive
cocc
obac
illus
;1-
to2-
mm
-dia
met
erno
nhem
olyt
icco
loni
escu
ltiv
ated
ontr
yptic
soy
agar
at30
°C;g
elat
inhy
drol
ysis
and
citr
acon
ate
nega
tive;
pro
duce
sac
idfr
omD
-glu
cose
;53%
ofst
rain
sut
ilize
tryp
tam
ine
15
Vibr
ioci
dici
isp
.nov
.Vi
brio
nace
aeBl
ood
(n�
3)N
otes
tab
lishe
dC
urve
d,m
otile
,oxi
dase
-pos
itive
Gra
m-n
egat
ive
bac
illus
;suc
rose
-fer
men
tativ
eco
loni
escu
ltiv
ated
onth
iosu
lfate
-citr
ate-
bile
salt
s-su
cros
eag
ar;g
row
thob
serv
edin
tryp
ticso
yb
roth
at30
°Cw
ithN
aCl
conc
entr
atio
nsup
to8%
for
mos
tis
olat
es;u
tiliz
esL-
rham
nose
asth
eso
leca
rbon
sour
ce;m
ost
isol
ates
dono
tut
ilize
sodi
umci
trat
e
16
Ente
roba
cter
horm
aech
eisu
bsp
.hor
mae
chei
sub
sp.
nov.
Ente
roba
cter
iace
aeSp
utum
(n�
2),t
hroa
t,b
lood
,gr
oin,
and
feca
lsa
mp
les,
asde
scrib
edin
refe
renc
e17
Not
esta
blis
hed
Gra
m-n
egat
ive
bac
illus
exhi
biti
ngge
nera
lch
arac
teris
tics
ofEn
tero
bact
ercl
oaca
eco
mp
lex;
dulc
itol
pos
itive
;ado
nito
l,D
-ara
bito
l,D
-sor
bito
l,an
dD
-mel
ibio
sene
gativ
e17
f
Ente
roba
cter
horm
aech
eisu
bsp
.oha
rae
sub
sp.n
ov.
Ente
roba
cter
iace
aeBl
ood
(n�
2),t
rach
ea(n
�2)
,b
ronc
hoal
veol
arla
vage
fluid
(n�
2),t
hroa
t(n
�2)
,fe
ces,
ear,
sput
um,m
outh
,ur
ine,
and
absc
ess
spec
imen
s,as
desc
ribed
pre
viou
sly
( 17)
Not
esta
blis
hed
Gra
m-n
egat
ive
bac
illus
exhi
biti
ngge
nera
lch
arac
teris
tics
ofth
eEn
tero
bact
ercl
oaca
eco
mp
lex;
Am
pC
hyp
erp
rodu
ctio
nin
25%
ofst
rain
sch
arac
teriz
edin
refe
renc
e17
;D
-sor
bito
lan
dD
-mel
ibio
sep
ositi
ve;a
doni
tol,
D-a
rab
itol,
and
dulc
itol
nega
tive
17f
Ente
roba
cter
horm
aech
eisu
bsp
.ste
iger
wal
tiisu
bsp
.no
v.
Ente
roba
cter
iace
aeW
ound
(n�
6),u
rine
(n�
5),
blo
od(n
�3)
,tra
chea
(n�
2),b
ronc
hoal
veol
arla
vage
fluid
,sp
utum
,lun
gb
iop
sy,
thro
at,v
agin
al,a
ndce
ntra
llin
esp
ecim
ens,
asde
scrib
edp
revi
ousl
y( 1
7)
Not
esta
blis
hed
Gra
m-n
egat
ive
bac
illus
exhi
biti
ngge
nera
lch
arac
teris
tics
ofEn
tero
bact
ercl
oaca
eco
mp
lex;
Am
pC
hyp
erp
rodu
ctio
nin
42%
ofst
rain
sch
arac
teriz
edin
refe
renc
e17
;pos
itive
adon
itol,
D-a
rab
itol,
D-s
orb
itol,
and
D-m
elib
iose
test
resu
lts;
nega
tive
dulc
itol
test
resu
lt
17f
(Con
tinue
don
next
pag
e)
Minireview Journal of Clinical Microbiology
February 2019 Volume 57 Issue 2 e01181-18 jcm.asm.org 4
on Decem
ber 4, 2020 by guesthttp://jcm
.asm.org/
Dow
nloaded from
TAB
LE1
(Con
tinue
d)
Scie
nti
ficn
ame
Fam
ilySo
urce
Clin
ical
rele
van
ceG
row
thch
arac
teri
stic
sRe
fere
nce
(s)
Citr
obac
ter
euro
paeu
ssp
.nov
.En
tero
bact
eria
ceae
Fece
sN
otes
tab
lishe
d;is
olat
efr
oma
U.S
.pat
ient
with
diar
rhea
Gra
m-n
egat
ive
bac
illus
exhi
biti
ngge
nera
lch
arac
teris
tics
ofCi
trob
acte
rsp
p.;
grow
thob
serv
edfr
om20
to50
°C;H
2S,
inos
itol,
and
salic
inp
ositi
ve;a
rgin
ine
dihy
drol
ase,
citr
ate,
sucr
ose,
and
star
chne
gativ
e
44
Sphi
ngob
acte
rium
cellu
litid
issp
.nov
.Sp
hing
obac
teria
ceae
Toe
Puru
lent
disc
harg
efr
oma
Kuw
aiti
cellu
litis
pat
ient
;nuc
leic
acid
hom
olog
yde
mon
stra
ted
with
pre
viou
sly
unna
med
Sing
apor
een
viro
nmen
tal
isol
ate
Aer
obic
,non
mot
ile,n
on-s
por
e-fo
rmin
g,ox
idas
e-p
ositi
veG
ram
-neg
ativ
eb
acill
us;0
.5-m
m-
diam
eter
pal
eye
llow
colo
nies
cult
ivat
edon
nutr
ient
,try
ptic
soy,
and
Mac
Con
key
agar
saf
ter
48h
ofin
cub
atio
nat
28–3
7°C
;cat
alas
e,Vo
ges-
Pros
kaue
r,tr
ypto
pha
nde
amin
ase,
and
�-g
alac
tosi
dase
pos
itive
;ure
ase,
deca
rbox
ylas
es,c
itrat
e,an
dni
trat
ene
gativ
e
45
Hae
mop
hilu
sm
assi
liens
issp
.no
v.Pa
steu
rella
ceae
Perit
onea
lflu
idIs
olat
efr
oma
Sene
gale
sefe
mal
ew
ithp
elvi
cp
erito
nitis
com
plic
atin
ga
rup
ture
dov
aria
nab
sces
s
Facu
ltat
ive,
nonm
otile
,non
-sp
ore-
form
ing,
oxid
ase-
pos
itive
Gra
m-n
egat
ive
bac
illus
;0.5
-to
1-m
m-d
iam
eter
nonh
emol
ytic
colo
nies
onb
lood
-enr
iche
dC
olum
bia
agar
;op
timal
grow
that
37°C
;alk
alin
ep
hosp
hata
se,l
euci
near
ylam
idas
e,an
dD
-glu
cose
utili
zatio
np
ositi
ve;i
ndol
ean
dD
-man
nose
utili
zatio
nne
gativ
e
46b
Wee
ksel
lam
assi
liens
issp
.nov
.Fl
avob
acte
riace
aeU
rine
Isol
ate
from
aSe
nega
lese
mal
ew
ithac
ute
cyst
itis
Aer
obic
,non
mot
ile,n
on-s
por
e-fo
rmin
g,ox
idas
e-p
ositi
veG
ram
-neg
ativ
eb
acill
us;l
ight
yello
w,2
-mm
-dia
met
er,s
moo
th,n
onhe
mol
ytic
colo
nies
onb
lood
-enr
iche
dC
olum
bia
agar
;alk
alin
ep
hosp
hata
se,l
euci
near
ylam
idas
e,an
dD
-xyl
ose
utili
zatio
np
ositi
ve;t
ryp
sin,
indo
le,u
reas
e,�
-gal
acto
sida
se,a
ndD
-glu
cose
utili
zatio
nne
gativ
e
47b
Ehrli
chia
mur
issu
bsp
.ea
ucla
irens
issu
bsp
.nov
.A
napl
asm
atac
eae
Who
leb
lood
Isol
ate
from
afe
bril
eW
isco
nsin
(USA
)p
atie
ntw
itha
hist
ory
oftic
kex
pos
ure
in20
09
Mor
pho
logi
can
dcu
ltur
alsi
mila
ritie
sto
E.m
uris
sub
sp.m
uris
sub
sp.n
ov.(
Tab
le2)
;ho
wev
er,E
.mur
issu
bsp
.euc
laire
nsis
sub
sp.n
ov.i
slo
caliz
edto
the
Uni
ted
Stat
es;t
heso
leve
ctor
isIx
odes
scap
ular
is,a
ndit
caus
eshu
man
dise
ase
48
King
ella
nege
vens
issp
. nov
.N
eiss
eria
ceae
Oro
pha
rynx
(n�
21)
Not
esta
blis
hed;
isol
ates
from
heal
thy
Isra
eli
and
Swis
sch
ildre
n
Non
mot
ile,n
on-s
por
e-fo
rmin
g,ox
idas
e-p
ositi
veG
ram
-neg
ativ
eco
ccob
acill
usth
atex
hib
itsca
pno
phi
licgr
owth
;pal
eye
llow
,bet
a-he
mol
ytic
0.5-
to1-
mm
-dia
met
erco
loni
eson
blo
od-e
nric
hed
Col
umb
iaag
ar;o
ptim
algr
owth
at37
°C;l
euci
near
ylam
idas
ep
ositi
ve;
urea
se,c
atal
ase,
indo
le,o
rnith
ine
deca
rbox
ylas
e,an
dp
rolin
ear
ylam
idas
ene
gativ
e
49
Psyc
hrob
acte
rpa
steu
riisp
.no
v.M
orax
ella
ceae
Hum
anor
igin
(n�
2);n
otot
herw
ise
spec
ified
Not
esta
blis
hed;
isol
ates
sub
mitt
edto
aFr
ench
colle
ctio
nb
ank
in19
72
Aer
obic
,non
mot
ile,n
on-s
por
e-fo
rmin
g,ox
idas
e-p
ositi
veG
ram
-neg
ativ
eco
ccob
acill
us;
optim
algr
owth
at30
°C;t
rans
luce
nt,b
right
,1-
to2-
mm
-dia
met
erco
loni
esob
serv
edon
blo
odag
ar;c
atal
ase,
urea
se,a
ndlip
ase
pos
itive
;red
uces
nitr
ate
toni
trite
;orig
inal
lyid
entifi
edas
am
emb
erof
the
Mor
axel
lage
nus
50
Psyc
hrob
acte
rpi
echa
udii
sp.
nov.
Mor
axel
lace
aeH
uman
orig
in(n
�4)
;not
othe
rwis
esp
ecifi
edN
otes
tab
lishe
d;is
olat
essu
bm
itted
toa
Fren
chco
llect
ion
ban
kin
1972
Aer
obic
,non
mot
ile,n
on-s
por
e-fo
rmin
g,ox
idas
e-p
ositi
veG
ram
-neg
ativ
eco
ccob
acill
us;
optim
algr
owth
at30
°C;t
rans
luce
nt,b
right
,1-
to2-
mm
-dia
met
erco
loni
esob
serv
edon
blo
odag
ar;c
atal
ase
pos
itive
;ure
ase
and
lipas
eac
tivity
isva
riab
le;u
nab
leto
redu
ceni
trat
eto
nitr
ite;o
rigin
ally
iden
tified
asa
mem
ber
ofth
eM
orax
ella
genu
s
50
Burk
hold
eria
sing
ular
issp
. nov
.Bu
rkho
lder
iace
aeRe
spira
tory
(n�
4)N
otes
tab
lishe
d;is
olat
esfr
omcy
stic
fibro
sis
pat
ient
sin
Can
ada
and
Ger
man
y
Aer
obic
,non
-sp
ore-
form
ing
Gra
m-n
egat
ive
bac
illus
;mot
ility
varia
ble
;gro
wth
onC
olum
bia
shee
pb
lood
agar
(muc
oid,
nonh
emol
ytic
colo
nies
),Bu
rkho
lder
iace
paci
aag
ar,y
east
extr
act
man
nito
lag
ar,a
ndM
acC
onke
yag
arat
42°C
;slo
wox
idas
eac
tivity
;aci
dific
atio
nof
gluc
ose,
mal
tose
,lac
tose
,and
xylo
seb
utno
tsu
cros
e;ni
trat
ere
duct
ion,
lysi
nede
carb
oxyl
ase,
and
orni
thin
ede
carb
oxyl
ase
nega
tive
51g
Shew
anel
laca
rass
iisp
.nov
.Sh
ewan
ella
ceae
Fece
sN
otes
tab
lishe
d;is
olat
efr
oma
Chi
nese
infa
ntw
ithdi
arrh
eaFa
cult
ativ
e,m
otile
,oxi
dase
-pos
itive
Gra
m-n
egat
ive
bac
illus
;gro
wth
onLB
agar
and
blo
odag
ar(h
emol
ytic
),w
ithop
timal
grow
that
35°C
;poo
rgr
owth
onM
acC
onke
yag
ar;
colo
nies
onLB
agar
are
pin
k-or
ange
with
a2-
to3-
mm
diam
eter
;cat
alas
e,H
2S,
nitr
ate
redu
ctio
n,an
dL-
pro
line
aryl
amid
ase
pos
itive
;ure
ase
and
orni
thin
ede
carb
oxyl
ase
nega
tive;
does
not
grow
in10
%N
aCl
52
Gra
m-p
ositi
vean
aero
bes
Selli
mon
asin
test
inal
isge
n.no
v.,s
p.n
ov.
Lach
nosp
irace
aeFe
ces
Not
esta
blis
hed;
isol
ated
from
afe
cal
sam
ple
from
ahe
alth
yKo
rean
wom
an
Gra
m-p
ositi
vedi
plo
cocc
us-s
hap
ed,o
blig
ate
anae
rob
e,no
n-sp
ore-
form
ing;
form
siv
ory
yello
wco
loni
es;g
row
thoc
curs
at25
–45°
C;t
heop
timal
grow
thte
mp
erat
ure
is37
°C;
mot
ile;H
2S,
indo
le,u
reas
e,an
des
culin
hydr
olys
isne
gativ
e;ac
idp
rodu
ctio
nfr
oma
varie
tyof
carb
ohyd
rate
s
53
Pept
onip
hilu
sca
toni
aesp
.nov
.Pe
pton
iphi
lace
aeFe
ces
Not
esta
blis
hed;
isol
ated
from
ahu
man
feca
lsa
mp
lein
sout
hern
Peru
Gra
m-p
ositi
ve,n
on-s
por
e-fo
rmin
gco
ccus
;ob
ligat
ean
aero
be;
colo
nies
onb
lood
agar
are
need
lep
oint
insi
ze,b
eige
,and
circ
ular
with
asm
ooth
surf
ace;
optim
algr
owth
at37
°C;
cata
lase
,ure
ase,
indo
le,a
ndni
trat
ene
gativ
e
54
Prop
ioni
bact
eriu
mna
mne
tens
esp
. nov
.Pr
opio
niba
cter
iace
aeBo
neIn
fect
edtib
ial
frac
ture
Gra
m-p
ositi
ve,n
on-s
por
e-fo
rmin
g,no
nmot
ile,p
leom
orp
hic
bac
illi;
anae
rob
ic;a
fter
6da
ysof
incu
bat
ion
colo
nies
are
circ
ular
,dom
esh
aped
,and
from
pal
ecr
eam
toor
ange
-sal
mon
;op
timal
grow
that
35°C
55
Aga
thob
acul
umbu
tyric
ipro
duce
nsge
n.no
v., s
p.n
ov.
Rum
inoc
occa
ceae
Fece
sN
otes
tab
lishe
d;re
cove
red
from
the
fece
sof
ahe
alth
y23
-yea
r-ol
dKo
rean
wom
an
Gra
m-p
ositi
ve,n
on-s
por
e-fo
rmin
gst
rict
anae
rob
e;gr
ows
optim
ally
at37
°Cin
the
pre
senc
eof
0.5%
NaC
l,p
H7;
nonm
otile
;cat
alas
ean
dox
idas
ene
gativ
e;b
utyr
ate
pro
duci
ng56
Buty
ricic
occu
sfa
ecih
omin
issp
.no
v.Cl
ostr
idia
ceae
Fece
sN
otes
tab
lishe
d;re
cove
red
from
the
fece
sof
ahe
alth
yhu
man
adul
t
Gra
m-p
ositi
veco
ccoi
d-sh
aped
orga
nism
s;no
nmot
ilew
ithou
tsp
ores
;ob
ligat
ely
anae
rob
ic;
colo
nies
may
app
ear
wax
yan
dye
llow
ish
afte
rgr
owth
at37
°Cfo
r72
h;in
dole
pos
itive
57
(Con
tinue
don
next
pag
e)
Minireview Journal of Clinical Microbiology
February 2019 Volume 57 Issue 2 e01181-18 jcm.asm.org 5
on Decem
ber 4, 2020 by guesthttp://jcm
.asm.org/
Dow
nloaded from
TAB
LE1
(Con
tinue
d)
Scie
nti
ficn
ame
Fam
ilySo
urce
Clin
ical
rele
van
ceG
row
thch
arac
teri
stic
sRe
fere
nce
(s)
Faec
alim
onas
umbi
licat
age
n.no
v.,s
p.n
ov.
Lach
nosp
irace
aeFe
ces
Not
esta
blis
hed;
reco
vere
dfr
omth
efe
ces
ofa
heal
thy
hum
anad
ult
Gra
m-p
ositi
veb
acill
iin
pai
rsor
chai
ns;o
blig
ate
anae
rob
e;no
nmot
ile;n
onp
igm
ente
d;m
ayfo
rmsp
ores
;col
onie
sha
vea
dep
ress
edce
nter
(um
bili
cate
);H
2S
pro
duce
d;in
dole
,ca
tala
se,a
ndur
ease
nega
tive
58
Mer
dim
onas
faec
isge
n.no
v.,
sp.n
ov.
Lach
nosp
irace
aeFe
ces
Not
esta
blis
hed;
reco
vere
dfr
omth
efe
ces
ofa
heal
thy
hum
anad
ult
Gra
m-p
ositi
vest
rictl
yan
aero
bic
;non
-sp
ore
form
ing;
cata
lase
,ind
ole,
and
oxid
ase
nega
tive;
colo
nies
are
ivor
yco
lore
dan
dgr
owop
timal
lyat
37°C
59
Mon
oglo
bus
pect
inily
ticus
gen.
nov.
, sp
.nov
.Ru
min
ococ
cace
aeFe
ces
Not
esta
blis
hed;
reco
vere
dfr
omth
efe
ces
ofa
27-y
ear-
old
heal
thy
wom
anliv
ing
inN
ewZe
alan
d
Gra
m-p
ositi
veco
cci
that
are
stric
tly
anae
rob
ic;c
atal
ase
pos
itive
;oxi
dase
nega
tive;
indo
lene
gativ
e;fe
rmen
tsp
ectin
;op
timum
grow
thb
etw
een
30an
d40
°C60
Gra
m-n
egat
ive
anae
rob
esA
naer
ospo
raho
ngko
ngen
sis
gen.
nov.
,sp
.nov
.Ve
illon
ella
ceae
Bloo
dN
otes
tab
lishe
d;is
olat
esfr
oman
asym
pto
mat
icin
trav
enou
sdr
ugab
user
Ob
ligat
ean
aero
bic
,slig
htly
curv
ed,m
ultip
le-s
por
e-fo
rmin
g,G
ram
-neg
ativ
eb
acill
us(u
pto
14�
min
leng
th);
yiel
dsp
inp
oint
,cat
alas
e-ne
gativ
e,no
nhem
olyt
icco
loni
eson
blo
odag
arfo
llow
ing
48h
ofin
cub
atio
nat
37°C
;rel
ativ
ely
iner
tb
ioch
emic
ally
18c
Meg
asph
aera
mas
silie
nsis
sp.
nov.
Veill
onel
lace
aeFe
ces
Not
esta
blis
hed;
isol
ate
from
anH
IV-p
ositi
vep
atie
ntO
blig
ate
anae
rob
ic,n
on-s
por
e-fo
rmin
g,no
nmot
ileG
ram
-neg
ativ
eco
ccob
acill
us;y
ield
sca
tala
se-n
egat
ive,
0.5-
to1.
0-m
m-d
iam
eter
colo
nies
onb
lood
-enr
iche
dC
olum
bia
agar
;op
timal
grow
that
37°C
;aci
dp
rodu
ctio
nfr
omso
rbito
lan
dar
abito
l
61c
Sedi
men
tibac
ter
hong
kong
ensi
ssp
.nov
.Pe
ptos
trep
toco
ccac
eaeh
Bloo
dIs
olat
edfr
oma
pat
ient
with
sep
ticsh
ock
and
mul
tiorg
anfa
ilure
seco
ndar
yto
colo
nca
rcin
oma
Ob
ligat
ean
aero
bic
,slig
htly
curv
ed,m
otile
,ter
min
al-s
por
e-fo
rmin
gG
ram
-neg
ativ
eb
acill
us;
yiel
dsp
inp
oint
colo
nies
onb
uffe
red
char
coal
yeas
tex
trac
tag
arfo
llow
ing
72h
ofin
cub
atio
nat
37°C
;gro
wth
onag
arut
ilizi
ngBa
ctec
anae
rob
icb
lood
cult
ure
bro
thun
der
anae
rob
icco
nditi
ons;
nogr
owth
onb
ruce
llaag
ar,b
rain
hear
tin
fusi
onm
ediu
m,o
rco
oked
mea
tm
ediu
m;c
atal
ase
and
indo
lep
ositi
ve;n
itrat
ere
duct
ion
nega
tive
62c
Die
lma
fast
idio
sage
n.no
v.,
sp.n
ov.
Erys
ipel
otric
hace
aeFe
ces
Not
esta
blis
hed
Ob
ligat
ean
aero
bic
,mot
ile,n
on-s
por
e-fo
rmin
gG
ram
-neg
ativ
eb
acill
us;0
.5-
to1.
0-m
m-
diam
eter
colo
nies
onb
lood
-enr
iche
dC
olum
bia
agar
;op
timal
grow
that
30°C
;esc
ulin
hydr
olys
isan
dac
idar
ylam
idas
ep
ositi
ve;m
anno
se,s
ucro
se,a
ndD
-glu
cose
utili
zatio
nne
gativ
e
63d
Prev
otel
laco
lora
nssp
.nov
.Pr
evot
ella
ceae
Wou
ndIs
olat
edin
the
cont
ext
ofa
pol
ymic
rob
ial
infe
ctio
nO
blig
ate
anae
rob
ic,n
onm
otile
,non
-sp
ore-
form
ing,
shor
tan
dp
leom
orp
hic
Gra
m-n
egat
ive
bac
illus
;aft
er2–
5da
ysof
incu
bat
ion
at35
–37°
C,1
-mm
-dia
met
erco
loni
esha
vew
eak
grey
ish
bro
wn
pig
men
t;co
loni
esde
velo
pto
ffee
bro
wn
pig
men
taf
ter
exte
nded
incu
bat
ion;
gluc
ose,
sucr
ose,
and
lact
ose
ferm
enta
tion
pos
itive
;cat
alas
e(1
5%H
2O
2)
and
indo
lene
gativ
e
64
Ruth
enib
acte
rium
lact
atifo
rman
sge
n.no
v.,
sp.n
ov.
Rum
inoc
occa
ceae
Fece
sN
otes
tab
lishe
d;is
olat
efr
oma
heal
thy
Russ
ian
mal
eO
blig
ate
anae
rob
ic,n
onm
otile
,non
-sp
ore-
form
ing
Gra
m-n
egat
ive
bac
illus
;non
hem
olyt
ic,
0.15
-to
0.40
-mm
-dia
met
erco
loni
esaf
ter
96h
ofin
cub
atio
non
EGag
arat
37°C
;bile
tole
rant
;gro
wth
can
be
stim
ulat
edb
y5
mg
hem
in,0
.5%
mal
tose
,and
2–3%
Oxg
all;
escu
linan
dst
arch
hydr
olys
isp
ositi
ve
65
Gab
onib
acte
rm
assi
liens
isge
n.no
v., s
p.n
ov.
Porp
hyro
mon
adac
eae
Fece
sN
otes
tab
lishe
d;is
olat
efr
oma
heal
thy
Gab
ones
em
ale
Ob
ligat
ean
aero
bic
,mot
ileG
ram
-neg
ativ
eco
ccob
acill
us;2
-mm
-dia
met
erw
hite
colo
nies
afte
rin
cub
atio
non
shee
pb
lood
-enr
iche
dC
olum
bia
agar
at37
°C;i
ndol
e,es
tera
se,
este
rase
lipas
e,an
dac
idp
hosp
hata
sep
ositi
ve;c
atal
ase,
oxid
ase,
alka
line
pho
spha
tase
,an
dlip
ase
nega
tive
66i
Four
nier
ella
mas
silie
nsis
gen.
nov.
,sp
.nov
.Ru
min
ococ
cace
aeFe
ces
Not
esta
blis
hed;
isol
ate
from
ahe
alth
yFr
ench
mal
eO
blig
ate
anae
rob
ic,n
onm
otile
,non
-sp
ore-
form
ing
Gra
m-n
egat
ive
bac
illus
;op
timal
grow
that
37°C
;1-m
m-d
iam
eter
colo
nies
exhi
bit
whi
tep
igm
ent;
cata
lase
,oxi
dase
,and
indo
lene
gativ
e;ni
trat
ere
duct
ase,
D-m
anno
se,a
ndm
alto
sep
ositi
ve;t
hem
ajor
shor
t-ch
ain
fatt
yac
idis
acet
icac
id
67
Alis
tipes
ihum
iisp
.nov
.Ri
kene
llace
aeFe
ces
Isol
ate
from
aFr
ench
fem
ale
with
anor
exia
nerv
osa;
clin
ical
sign
ifica
nce
not
esta
blis
hed
Ob
ligat
ean
aero
bic
,non
-sp
ore-
form
ing,
nonm
otile
Gra
m-n
egat
ive
bac
illus
;op
timal
grow
that
37°C
;tra
nslu
cent
0.2-
mm
-dia
met
erco
loni
eson
blo
od-e
nric
hed
Col
umb
iaag
ar;l
eucy
lgl
ycin
ear
ylam
idas
e,ra
ffino
se,a
ndm
anno
sep
ositi
ve;u
reas
e,in
dole
,cat
alas
e,an
dni
trat
ere
duct
ase
nega
tive
68b
Bact
eroi
des
kore
ensi
ssp
.nov
.Ba
cter
oida
ceae
Fece
sN
otes
tab
lishe
d;is
olat
efr
oma
heal
thy
adul
tO
blig
ate
anae
rob
ic,n
onm
otile
,non
-sp
ore-
form
ing
Gra
m-n
egat
ive
bac
illus
;op
timal
grow
that
37°C
;sm
ooth
,cre
amy,
1-m
m-d
iam
eter
colo
nies
onre
info
rced
clos
trid
ial
med
ium
;gr
ows
inth
ep
rese
nce
ofb
ile;s
imila
rb
ioch
emic
alan
dfa
tty
acid
pro
file
asBa
cter
oide
skr
ibbi
sp.n
ov.,
with
the
exce
ptio
nof
nega
tive
reac
tions
for
�-g
luco
sida
sean
dgl
utam
icac
idde
carb
oxyl
ase
69
Bact
eroi
des
krib
bisp
.nov
.Ba
cter
oida
ceae
Fece
sN
otes
tab
lishe
d;is
olat
efr
oma
heal
thy
adul
tO
blig
ate
anae
rob
ic,n
onm
otile
,non
-sp
ore-
form
ing
Gra
m-n
egat
ive
bac
illus
;op
timal
grow
that
37°C
;sm
ooth
,cre
amy,
1-m
m-d
iam
eter
colo
nies
onre
info
rced
clos
trid
ial
med
ium
;gr
ows
inth
ep
rese
nce
ofb
ile;s
imila
rb
ioch
emic
alan
dfa
tty
acid
pro
file
asBa
cter
oide
sko
reen
sis
sp.n
ov.,
with
the
exce
ptio
nof
pos
itive
reac
tions
for
�-g
luco
sida
sean
dgl
utam
icac
idde
carb
oxyl
ase
69
(Con
tinue
don
next
pag
e)
Minireview Journal of Clinical Microbiology
February 2019 Volume 57 Issue 2 e01181-18 jcm.asm.org 6
on Decem
ber 4, 2020 by guesthttp://jcm
.asm.org/
Dow
nloaded from
TAB
LE1
(Con
tinue
d)
Scie
nti
ficn
ame
Fam
ilySo
urce
Clin
ical
rele
van
ceG
row
thch
arac
teri
stic
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fere
nce
(s)
Spiro
chet
esH
aem
atos
piril
lum
jord
ania
ege
n.no
v.,s
p.n
ov.
Rhod
ospi
rilla
ceae
Bloo
d(n
�14
)C
linic
aldi
agno
ses
ofse
ptic
emia
(n�
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db
acte
rem
ia(n
�1)
pro
vide
din
sele
ctin
stan
ces
Mot
ile,h
elic
alG
ram
-neg
ativ
eb
acte
rium
with
dim
ensi
ons
of1.
6�
mb
y0.
1–0.
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m;1
-mm
-di
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ithsl
ight
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emol
ysis
cult
ivat
edon
hear
tin
fusi
onag
arsu
pp
lem
ente
dw
ith5%
rab
bit
blo
odaf
ter
48h
ofin
cub
atio
nat
35°C
;cat
alas
e,ox
idas
e,an
dhy
drog
ensu
lfide
pos
itive
;ure
ase,
nitr
ate
redu
ctio
n,an
din
dole
nega
tive
70,7
1e
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elia
may
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sp.n
ov.
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chae
tace
aeBl
ood
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ynov
ial
fluid
Clin
ical
sign
ifica
nce
isde
scrib
edin
refe
renc
e72
Mot
ilesp
iroch
etes
cult
ivat
edfr
omb
lood
spec
imen
sut
ilizi
ngBa
rbou
r-St
oenn
er-K
elly
med
ium
ina
34°C
mic
roae
rop
hilic
envi
ronm
ent;
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ayon
ii-sp
ecifi
cnu
clei
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tect
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omIx
odes
scap
ular
istic
ksco
llect
edin
Wis
cons
inan
dM
inne
sota
(USA
)
73
aO
ther
mem
ber
sof
the
Paen
ibac
illac
eae
have
bee
nre
por
ted
tob
eG
ram
pos
itive
,Gra
mne
gativ
e,or
Gra
mva
riab
le.
bTa
xono
mic
desi
gnat
ion
sub
sequ
entl
yad
ded
inva
lidat
ion
list
no.1
76(7
4).
c Tax
onom
icde
sign
atio
nsu
bse
quen
tly
adde
din
valid
atio
nlis
tno
.168
(11)
.dTa
xono
mic
desi
gnat
ion
sub
sequ
entl
yad
ded
inva
lidat
ion
list
no.1
70(7
5).
e Tax
onom
icde
sign
atio
nsu
bse
quen
tly
adde
din
valid
atio
nlis
tno
.171
(76)
.f T
axon
omic
desi
gnat
ion
sub
sequ
entl
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TABLE 2 Revised bacterial taxa from January 2016 through December 2017
Former name Revised name Other information Reference(s)
Gram-positive cocciStreptococcus oralis
emendeddescription
The main characteristics are those provided in references 80 and 81, with theaddition that some strains hydrolyze arginine
82
Streptococcus oralissubsp. oralissubsp. nov.
Closely related species to S. oralis in the mitisgroup have been reclassified as subspecies ofS. oralis
S. oralis subsp. oralis was created; all strains produce IgA1 protease andextracellular polysaccharide; they do not hydrolyze arginine
82
Streptococcusdentisani
Streptococcus oralis subsp. dentisani comb. nov. The description is the same as that provided in reference 83, with theaddition that it does not produce IgA1 protease or extracellularpolysaccharide; most strains possess �-galactosidase; strains have beenisolated from the dorsum of the tongue and human caries-free toothsurfaces
82
Streptococcustigurinus
Streptococcus oralis subsp. tigurinus comb. nov. The description is the same as that provided in reference 84, with theaddition that most strains possess the enzyme �-galactosidase and allpossess the gene for N-acetyl-�-glucosaminidase; strains have beenisolated from human blood
82
Gram-positive bacilliBrevibacterium
massilienseBrevibacterium ravenspurgense emended The previous taxonomic status of B. massiliense is described in reference 85;
organism originally isolated from ankle discharge86
Arthrobactersanguinus
Haematomicrobium sanguinus gen. nov., comb.nov.
Original isolation from blood culture is described in reference 87; it has alsocaused peritonitis in a dialysis patient (88)
89
Gram-negative bacilliAchromobacter
spiritinusAchromobacter marplatensis Taxonomy revision related to previous erroneous report of sequence data;
the previous taxonomy of A. spiritinus is described in references 1, 90, and91; clinical relevance in humans is not established
92
Acinetobactergenomicspecies 14BJ
Acinetobacter courvalinii sp. nov. Human strains include those isolated from skin and soft tissue (n � 3), blood(n � 1), urine (n � 1), conjunctiva (n � 1), and tracheal aspirate(n � 1) specimens; the previous designation is described in references 93and 94; the clinical relevance of all isolates could not be ascertained
19
Acinetobactergenomicspecies 17
Acinetobacter dispersus sp. nov. Human strains include those isolated from skin and soft tissue specimens(n � 3) and an unknown source (n � 1); the previous designation isdescribed in reference 93; the clinical relevance of all isolates could not beascertained
19
Acinetobactertaxon 18
Acinetobacter modestus sp. nov. Human strains include those isolated from blood (n � 2), throat (n � 1),urine (n � 1), and skin and soft tissue (n � 1) specimens; the previousdesignation is described in references 94 to 96; the clinical relevance of allisolates could not be ascertained
19
Acinetobactertaxon 19
Acinetobacter proteolyticus sp. nov. Human isolates from skin and soft tissue (n � 4), blood (n � 1), and ear(n � 1) specimens; the previous designation is described in reference 93;the clinical relevance of all isolates could not be ascertained
19
Acinetobactertaxon 20
Acinetobacter vivianii sp. nov. Human strains include those isolated from blood (n � 2) and skin and softtissue (n � 1) specimens and an unknown source (n � 1); the previousdesignation is described in references 93 and 94; the clinical relevance ofall isolates could not be ascertained
19
Klebsiella alba Klebsiella quasipneumoniae subsp.similipneumoniae
K. alba was originally isolated from a polluted soil sample in China, with thetaxonomy previously published (97) and added (98); the taxonomic statusand clinical significance of K. quasipneumoniae subsp. similipneumoniaehuman isolates are discussed elsewhere (1, 99)
100
Capnocytophagacanimorsus(selectedstrains)
Capnocytophaga canis sp. nov. Subset of less virulent C. canimorsus strains not isolated from humaninfections has been given a novel species designation; the C. canimorsusdesignation is reserved for species including human pathogens
101a
Paraburkholderiazhejiangensis
Caballeronia zhejiangensis comb. nov. The initial designation of Burkholderia zhejiangensis was published inreference to a wastewater isolate (102) and augmented by three clinicalisolates (blood, respiratory secretions) (103); the intermediate taxonomicstatus of P. zhejiangensis was previously published (104) and added (105)
20
Helicobactercinaedi(selectedstrains)
Helicobacter canicola sp. nov. Subset of H. cinaedi strains not isolated from human infections has beengiven a novel species designation
106b
Rhizobium pusense Agrobacterium pusense comb. nov. The initial designation of R. pusense was published in reference to arhizosphere isolate (107); the pathogenicity of R. pusense (and the previousreclassification of other Agrobacterium spp. as R. pusense) in humaninfections is described in reference 108
21b
Agrobacterium sp.genomovar G2
Agrobacterium pusense comb. nov. Isolated from human blood 21b,c
Elizabethkingiaendophytica
Elizabethkingia anophelis Clinical relevance not established in humans; the previous designation of E.endophytica is described in reference 109; E. endophytica is no longerconsidered a separate species of the genus Elizabethkingia
110
Rahnellagenomospecies2
Rahnella variigena sp. nov. Taxonomic status previously discussed in reference 1 111d
Enterobacteraerogenes
Klebsiella aerogenes comb. nov. Taxonomic status previously discussed in reference 112 113
(Continued on next page)
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Novel taxa. Of the two novel genera that fall into the “Gram-positive cocci” groupin Table 1, the most interesting is Streptococcus halichoeri subsp. hominis. Streptococcushalichoeri was originally isolated from gray seals (Halichoerus grypus) in 2004 in theUnited Kingdom (25). Subsequent to the description of this organism, isolates that wereassociated with infections in humans (four from blood and one from a sinus) and thatwere sent to the Centers for Disease Control and Prevention (CDC) were found to bephenotypically similar to S. halichoeri (26). In 2014, an additional isolate was recoveredfrom a man with empyema in Singapore (27). None of these patients were believed tohave an association with seals or ocean water; the average age of the patients was63 years, and they were from different geographic locations (26). In a comprehensiveinvestigation of the human isolates of S. halichoeri, the six isolates were characterizedby Shewmaker et al. (26) using whole-genome and targeted gene sequencing and avariety of phenotypic methods. The six human isolates were genetically and pheno-typically identical and most closely related to S. halichoeri. They can be distinguishedfrom the type strain recovered from a seal as follows: positive for bile esculin andesculin hydrolysis, positive for acid production from sucrose, and positive for�-glucosidase, �-glucuronidase, and acid production from methyl-�-D-glucopyranoside(Rapid ID32 test system [bioMérieux, Inc., Durham, NC]) (26). On the basis of bothphenotypic and genotypic differences from the seal type strain, the human isolates arebelieved to be a subspecies of S. halichoeri and are referred to as S. halichoeri subsp.hominis. Strains from marine animals are referred to as S. halichoeri subsp. halichoeri.
Two new Gram-positive aerobic bacilli associated with ocular infections have beenadded to the genus Corynebacterium. Corynebacterium lowii and Corynebacterium oculi
TABLE 2 (Continued)
Former name Revised name Other information Reference(s)
Herbaspirillummassiliense
Noviherbaspirillum massiliense comb. nov. Isolation from feces of a healthy Senegal patient, with the initial taxonomicstatus previously described in references 1, 114, and 115
116, 117
[Pasteurella]pneumotropica
Rodentibacter pneumotropicus comb. nov. Official 16S rRNA-based taxonomic designation granted for (misclassified) [P.]pneumotropica; human respiratory tract isolates are described in reference118
119
Ehrlichia muris Ehrlichia muris subsp. muris subsp. nov. Clinical significance in humans not definitively established; serologic evidenceof human infection in Japan (120)
48
Acinetobactergenospecies 13
Acinetobacter colistiniresistens sp. nov. Isolation previously described in reference 93 121
Acinetobacter DNAgroup 14
Acinetobacter colistiniresistens sp. nov. Isolation previously described in reference 122 121
Burkholderiaconcitans
Caballeronia concitans comb. nov. Isolation and proposed taxonomic status previously published (14) andadded (76)
123
Burkholderiaturbans
Caballeronia turbans comb. nov. Isolation and proposed taxonomic status previously described (14) andadded (76)
123
Enterobactermassiliensis
Metakosakonia massiliensis comb. nov. Previous taxonomic status of E. massiliensis described in references 1 and 124 125e
Escherichia vulneris Pseudescherichia vulneris comb. nov. Previous taxonomic status of E. vulneris described in reference 126 125e
Gram-positiveanaerobes
Propionibacteriumacnes
Cutibacterium acnes comb. nov. The description is the same as that provided in reference 127 128, 129
Propionibacteriumavidum
Cutibacterium avidum comb. nov. The description is the same as that provided in reference 127
Propionibacteriumgranulosum
Cutibacterium granulosum comb. nov. The description is the same as that provided in reference 127
Propionibacteriumpropionicum
Pseudopropionibacterium propionicum comb. nov. The description is the same as that provided in reference 127; the specieshas been associated with abscesses at a variety of different sites (psoas,brain)
128
Clostridium difficile Clostridioides difficile gen. nov., comb. nov. The description is identical to that for Clostridium difficile (130) 131Clostridium
mangenotiiClostridioides mangenotii comb. nov. The description of Clostridioides mangenotii is identical to that provided in
reference 132Eubacterium
contortumFaecalicatena contorta gen. nov., comb. nov. A previous description of Eubacterium contorta can be found in reference
133; Faecalicatena spp. are obligately anaerobic Gram-positive bacilli foundin chains or pairs; nonmotile; may or may not form spores; F. contortagrows optimally at 37°C
58
aTaxonomic designation subsequently added in validation list no. 170 (75).bTaxonomic designation subsequently added in validation list no. 172 (77).cX. Nesme, personal communication.dTaxonomic designation subsequently added in validation list no. 174 (134).eTaxonomic designation subsequently added in validation list no. 178 (78).
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were recovered primarily from patients in Japan at the time of ocular surgery and/orfrom patients with conjunctivitis (32). At the time of recovery from clinical material, theywere described as high-level fluoroquinolone-resistant isolates distinguishable fromCorynebacterium macginleyi (32). Additional characterization found them to be novelspecies.
Another noteworthy novel genus and species listed with the aerobic Gram-positivebacilli is Lawsonella clevelandensis gen nov., sp. nov. This is a very unusual organism, inthat it grows best anaerobically, requiring prolonged incubation, yet it is modifiedacid-fast positive and beaded and branching on Gram stain and by sequencing is mostclosely related to members of the genus Dietzia (33, 34). In the original paper describingthese infections, patients from Cleveland, Ohio, Winnipeg, Manitoba, Canada, and NewYork City had significant abscess collections of the spine (hardware associated), breast,and liver, respectively (34). Three of the patients were immunocompromised, anddiabetes was a significant comorbid factor. Because of the fastidious nature of theorganism growth, susceptibility testing could not be performed. Two of the patientsresponded to a combination of abscess drainage and amoxicillin-clavulanate; the otherpatients received regimens that included trimethoprim-sulfamethoxazole (34). Two
TABLE 3 Update on clinical relevance for selected new taxonomy described previously in JCM in 2017
OrganismSource previously reported inJCM (1) Updated clinical relevance Reference
Streptococcus dentisani Caries-free human tooth surfaces Infective endocarditis; refer to Table 2 for current taxonomic status 135Staphylococcus argenteus Lymph node drainage Purulent lymphadenitis in a Japanese boy 136Gemella taiwanensis Blood Infective endocarditis in a woman with dental caries 137Nocardia kroppenstedtii Brain abscess, blood Immunocompromised patient who presented with central nervous
system symptoms; the patient was found to have brainabscesses and endocarditis
138
Achromobacter animicus Sputum Multidrug-resistant organism implicated in wound infection inTanzania
139
Burkholderiapseudomultivorans
Sputum Bacteremia (not otherwise specified) 140
Klebsiella quasipneumoniaesubsp. quasipneumoniae
Type strain derived from blood Biliary tract infection 141
Liver abscess 142Urinary tract infection (n � 2) 143
Klebsiella quasipneumoniaesubsp. similipneumoniae
Type strain derived from blood Extended-spectrum �-lactamase-producing urine culture isolate 144
Sepsis (necrotizing fasciitis source) 145Clinical isolates from Malaysia (not otherwise specified) harboring
CTX-M, TEM, and NDM resistance determinants146
Odontogenic infection 147Nosocomial infection isolates from Brazil (not otherwise specified)
harboring KPC-2 and OKP-B-6 resistance determinants148
Acinetobacter variabilis Urine, feces, ocular, blood, leg,peritoneal dialysis fluid, toe
Neonatal sepsis in India 149
Sputum from cystic fibrosis patients in Brazil 150Acinetobacter seifertii Blood, ulcer, respiratory Catheter-related bloodstream infection 151
Sputum from cystic fibrosis patients in Brazil 150Ten isolates characterized, including urine culture isolate from
elderly female with dizziness152
Catheter-related sepsis in pediatric patient; pressure ulcer; intra-abdominal abscess
153
Archived tracheal aspirate and nasal secretion isolates from 1993and 1997 harboring OXA-58 resistance determinant
154
Christensenella minuta Feces Coisolated with Desulfovibrio desulfuricans from blood of patientwith acute appendicitis
155
Eisenbergiella tayi Blood Canadian study of eight blood culture isolates and one appendixtissue culture isolate (also with positive blood culture)
156
Klebsiella michiganensis Toothbrush holder Isolate harboring KPC-2, NDM-1, and NDM-5 resistancedeterminants recovered from immunocompromised Chinesepatient with acute diarrhea
157
Actinotignum spp. Blood Bacteremia among elderly patients 158
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additional cases of infection caused by L. clevelandensis have been reported. The firstoccurred in a patient with ulcerative colitis and a right lower quadrant intra-abdominalabscess (35). Because of the acid-fast nature of the organism, the patient was initiallythought to have intra-abdominal tuberculosis. However, subsequent 16S rRNA genesequencing performed on the abscess fluid identified the organism as L. clevelandensis,and the patient responded well to amoxicillin-clavulanate and drainage of the abscess(35). A very recent case report involved a 29-year-old woman who had a breast nodulethat yielded a Gram-positive filamentous organism identified by molecular methods asL. clevelandensis (159).
With respect to Gram-negative organisms, three valid subspecies of Enterobacterhormaechei (namely, Enterobacter hormaechei subsp. hormaechei subsp. nov., Entero-bacter hormaechei subsp. oharae subsp. nov., and Enterobacter hormaechei subsp.steigerwaltii subsp. nov.) have been officially added by IJSEM (17, 77), though clinicaldata were not provided to ascribe true clinical relevance. A novel Enterobacter spp.,Enterobacter bugandensis sp. nov. (39), was isolated from 17 neonates in a Tanzaniansepsis outbreak. These isolates tested resistant to fluoroquinolones, aminoglycosides,and tetracycline and harbored the CTX-M-15 resistance determinant. A pair of faculta-tive Gram-negative bacilli, Citrobacter europaeus sp. nov. (44) and Shewanella carassii sp.nov. (52), have been isolated from individuals with diarrhea.
The nonmotile coccobacillus Alkanindiges hongkongensis sp. nov. was isolated froma Chinese patient with an infected Warthin’s tumor that resulted in a parotid glandabscess and peripheral leukocytosis (11, 40). The patient responded well to surgicaldrainage of the abscess and a course of amoxicillin-clavulanate. Organism growth wassignificantly enhanced by Tween 80 supplementation. The oxidase-positive, Gram-negative bacillus Sphingobacterium cellulitidis sp. nov. (45) was isolated from a patientwith cellulitis in Kuwait. The erythematous and purulent infection resolved following a1-week amoxicillin-clavulanate regimen. During genetic characterization of the clinicalisolate, homology with a previously unnamed activated sludge isolate derived fromSingapore was demonstrated.
A novel member of the Anaplasmataceae, Ehrlichia muris subsp. eauclairensis subsp.nov. (48), was isolated from an upper midwestern United States febrile patient withprevious Ixodes scapularis tick exposure. This subspecies is now delineated fromEhrlichia muris subsp. muris subsp. nov. (Table 2), in that the latter has been recoveredfrom multiple genera of ticks, involves multiple natural reservoir hosts, and has distri-bution in Eastern Europe and Japan. Furthermore, human clinical disease with an E.muris subsp. muris subsp. nov. etiology has not been definitively established, thoughserologic evidence of a human immune response has been reported from Japan (120).
Only one of the new species listed under the Gram-positive anaerobes category inTable 1 was recovered from a clinical infection. Propionibacterium namnetense sp. nov.was isolated from a patient who had an infected tibial fracture (55). The remainingnovel genera and species were recovered from the feces of otherwise healthy humansin many cases during the study of intestinal microbiomes. Similarly, many of the novelanaerobic Gram-negative agents have not had clinical significance established, thoughMegasphaera massiliensis sp. nov. (11, 61) was isolated from an HIV-positive patient andSedimentibacter hongkongensis sp. nov. (11, 62) was recovered from a patient withseptic shock and multiorgan failure.
With respect to spirochetes, the valid name of Haematospirillum jordaniae gen. nov.,sp. nov. (70, 71), was added by IJSEM in 2016 (76). The type strain was derived fromhuman blood and referred to CDC in 2010. During a brief interval in 2012, 3 isolateswith identical 16S rRNA sequences matching those of both the type strain and 10previously characterized (but unnamed) isolates were forwarded to CDC. All isolateswere derived from men (mean age, 60 years), and the clinical diagnoses ranged fromsepticemia to tularemia. Limited clinical data were available (70), though two patientsreported headache, fever, chills, diarrhea, and swelling in the lower extremities.
Routine Borrelia burgdorferi sensu lato oppA1 PCR testing performed at an uppermidwestern United States reference laboratory revealed six clinical specimens (five
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blood specimens and one synovial fluid specimen from six patients) with atypicalmelting curve profiles (72). Subsequent sequencing of amplified 16S rRNA, in part,resulted in the characterization of the novel taxon Borrelia mayonii sp. nov. (73). Fieldsurveys in Wisconsin and Minnesota recovered I. scapularis ticks from which B. mayoniisp. nov. DNA was detected by PCR. This form of spirochetal disease differed from typicalLyme borreliosis paradigms in several facets (72). In the limited data set, the novelagent was detected more frequently from blood specimens than from synovial fluidspecimens. To an extent, these data were corroborated by higher median oppA1 copynumbers and profound spirochetemia (as observed by microscopy) compared to thosein infections caused by B. burgdorferi sensu stricto. Finally, clinical presentations in-cluded findings of diffuse macular rash not consistent with erythema migrans, nauseaand vomiting, and high-grade fever. Several symptoms more closely resembled thoseassociated with relapsing fever borrelial disease (160).
Taxonomic revisions. In the previous taxonomic update in this journal published in2017, a novel Streptococcus species, Streptococcus tigurinus, was highlighted (1). Zbin-den et al. (84) described this organism as causing serious and invasive infections,including bacteremia and endocarditis. In 2016, this organism was reclassified as asubspecies of Streptococcus oralis (Table 2) (82). Streptococcus oralis now has threesubspecies: S. oralis subsp. oralis, S. oralis subsp. dentisani, and S. oralis subsp. tigurinus(82). S. oralis subsp. dentisani comb. nov. has been reported as a cause of infectiveendocarditis (Table 3) (135).
In 1971, Bascomb et al. (161) characterized a subset of Enterobacter aerogenes strainsthat more closely resembled Klebsiella spp. from a phenotypic perspective. At that time,taxonomic transfer to Klebsiella aerogenes was not possible and the taxon Klebsiellamobilis was utilized for naming this species. It was subsequently determined bytaxonomists (113) that this nomenclature convention was illegitimate. Moreover, byway of adherence to contemporary nomenclature code (162), it was determined thatthe name Klebsiella aerogenes was available for use. Thus, E. aerogenes has now beentransferred to Klebsiella aerogenes comb. nov. (Table 2) (113) and K. mobilis is ahomotypic synonym of Klebsiella aerogenes comb. nov. The clinical utility of thistaxonomic revision remains to be seen, particularly with respect to salient differencesin the predicted antimicrobial susceptibility profiles of the Klebsiella and Enterobactergenera in general (particularly relevant to cephamycins, first-generation cephems, and�-lactam–�-lactamase inhibitor combinations, such as ampicillin-sulbactam [163]) andthe confusion that this may present to clinicians.
In a publication not included in Table 2, Adeolu et al. (164) used comparativegenomic analyses based on greater than 1,500 core proteins, 53 ribosomal proteins,and 4 multilocus sequence analysis proteins to reorganize families and genera withinwhat is now known as Enterobacteriales ord. nov. Essentially, six new families have beencreated from the family Enterobacteriaceae. These new families and the inclusive generaare Erwiniaceae fam. nov. (containing the genera Erwinia, Buchnera, Pantoea, Phaseoli-bacter, Tatumella, and Wigglesworthia), Pectobacteriaceae fam. nov. (containing thegenera Pectobacterium, Brenneria, Dickeya, Lonsdalea, and Sodalis), Yersiniaceae fam.nov. (containing the genera Yersinia, Chania, Ewingella, Rahnella, Rouxiella, Samsonia,and Serratia), Hafniaceae fam. nov. (containing the genera Hafnia, Edwardsiella, andObesumbacterium), Morganellaceae fam. nov. (containing the genera Morganella, Ar-senophonus, Cosenzaea, Moellerella, Photorhabdus, Proteus, Providencia, and Xenorhab-dus), and Budviciaceae fam. nov. (containing the genera Budvicia, Leminorella, andPragia). The remaining Enterobacteriales genera remain in an emended description ofthe family Enterobacteriaceae (164).
Perhaps the most clinically impactful changes have been among the genera Clos-tridium and Propionibacterium. The group of propionibacteria associated with the skinbiome of human hosts constitutes a distinct clade in the genus Propionibacterium.Whole-genome sequencing and more sophisticated phylogenetic analyses supportplacing the species associated with human skin into a new genus, Cutibacterium. The
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novel Cutibacterium genus includes the species Cutibacterium acnes, C. avidum, and C.granulosum previously assigned to the Propionibacterium genus (Table 2) (128). Thenovel genus Pseudopropionibacterium now contains the species formerly called Propi-onibacterium propionicum (Table 2) (128). Several of the propionibacteria associatedwith dairy sources, such as matured cheeses, have been placed into the genusAcidipropionibacterium gen. nov. (refer to reference 128 for more details about dairystrains). As also inferred with the Klebsiella aerogenes (Enterobacter aerogenes) para-digm, the clinical microbiologist may wish to consult with clinical practitioner col-leagues regarding the optimal manner to report the identification of organisms af-fected by taxonomic revisions. With respect to the former Propionibacterium acnes,possibilities may include “Cutibacterium acnes (formerly Propionibacterium acnes)” or“Cutibacterium acnes (formerly P. acnes).”
The genus Clostridium is also undergoing substantial changes. Application of mo-lecular methods, including complete sequencing of the 16S rRNA gene and othermethods, emphasizes the phylogenetic diversity of this group of organisms and has ledto the decision to reserve the genus designation of Clostridium sensu stricto to rRNAcluster I, which includes the type species Clostridium butyricum (131, 165). Conse-quently, the majority of Clostridium species which are not consistent with the genusClostridium description, as emended by Lawson and Rainey (165), will be assigned toother genera. Clostridium difficile is phylogenetically distant from cluster I and is locatedin cluster XI (131). Phylogenetic studies have shown that the type strain of C. difficilebelongs in the family Peptostreptococcaceae. In 2013, Yutin and Galperin (166) proposedcreating a new genus, Peptoclostridium, to accommodate the Clostridium species reas-signed to the family Peptostreptococcaceae. This proposal, which would have placedmany diverse species into a single genus (including C. difficile), was rejected as beingtoo simplistic (167). Subsequently, with the recognition that the proposed namePeptoclostridium difficile would change the monikers of C. difficile or C diff alreadyingrained in commercial products, packaging, computer systems, and clinical labora-tories and to avoid tremendous confusion among clinicians, Lawson and colleagues(131) proposed a compromise with the new designation of Clostridioides difficile,thereby retaining the abbreviation commonly used for C. difficile. It is hoped that thisdesignation will mitigate the time and cost associated with the required reclassification,as oftentimes only the abbreviation is used. The only other species in this new genusis Clostridioides mangenotii. Changes to other genera not highlighted here have beenmade or are forthcoming. Many of these new genera contain species not associatedwith human infections. In the 2017 minireview, we highlighted the reassignment ofClostridium hathewayi into the new genus Hungatella as Hungatella hathewayi gen.nov., comb. nov., in 2014 (1). A resident of the human intestinal tract, this organism hasbeen associated with surgical site infections and bacteremia (reviewed in reference168). Like other clostridia, it may stain Gram negative.
One major paradigm of bacterial taxonomy revision was, unfortunately, overlookedin our first compendium. Adeolu and Gupta (169) proposed a reclassification of Borreliasp. spirochetes in 2014. Agents responsible for Lyme disease (formerly residing in theBorrelia burgdorferi sensu lato complex) were transferred to Borreliella gen. nov., whilespirochetal agents largely responsible for relapsing fever retained the Borrelia genusdesignation (type species, Borrelia anserina). Per Adeolu and Gupta (169), specificagents within Borreliella gen. nov. include Borreliella burgdorferi comb. nov. (the typespecies of Borreliella), B. afzelii comb. nov., B. americana comb. nov., B. bavariensis comb.nov., B. carolinensis comb. nov., B. garinii comb. nov., B. japonica comb. nov., B.kurtenbachii comb. nov., B. lusitaniae comb. nov., B. sinica comb. nov., B. spielmaniicomb. nov., B. tanukii comb. nov., B. turdi comb. nov., and B. valaisiana comb. nov. Validnames of B. bavariensis, B. burgdorferi, B. carolinensis, B. garinii, B. japonica, B. kurten-bachii, B. sinica, and B. spielmanii have been added by IJSEM (170), yet this topic remainsthe subject of controversy and discussion (171, 172). To our knowledge, the nomen-clature of the novel taxon Borrelia mayonii sp. nov. (Table 1) has not been revised.
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Recently ascribed clinical significance. New literature on novel Gram-positive taxahighlighted in the original series (1) is summarized here and in Table 3. A case ofpurulent lymphadenitis attributed to Staphylococcus argenteus was reported in aJapanese child (136). The authors highlight the observations that this organism is oftenmisidentified as nonpigmented S. aureus. Up to this time, most human cases have beenfound in northeastern Thailand (136). The first case report of infective endocarditiscaused by Gemella taiwanensis was published by Hikone et al. (137). In contrast to thecases mentioned in the initial description of this organism (173), this patient was notimmunocompromised, and it is believed that her native valve endocarditis occurredafter extensive treatment for dental caries (137). The first reported case of disseminatedNocardia kroppenstedtii was reported by Majeed et al. (138). This patient was animmunocompromised gentleman (mantle cell lymphoma) who presented with newcentral nervous system symptoms. He was found to have brain abscesses as well as amitral valve mass. Blood cultures and a brain biopsy specimen were positive for N.kroppenstedtii (138). Finally, with respect to the Gram-positive anaerobes, much newliterature on Actinotignum schaalii can be found via PubMed primary literaturesearches, and the interested reader is directed there for those papers. A comprehensivereview highlighting the clinical and microbiological features of Actinotignum spp. isreferenced (158), with the authors noting that Actinotignum bacteremia affects elderlypersons with comorbidities and is associated with high mortality.
Particular clinical significance can be ascribed to several taxa listed in Table 3 on thebasis of multidrug resistance (139, 144, 146, 148, 149, 154, 157). One of these genus/species designations, Klebsiella quasipneumoniae, is frequently misidentified by theclinical microbiology laboratory as Klebsiella pneumoniae (174), yet it has the potentialto harbor similar resistance determinants and virulence factors as K. pneumoniae. Elliottet al. (175) published the whole-genome sequence of the commonly utilized qualitycontrol strain ATCC 700603, identifying it as K. quasipneumoniae subsp. similipneu-moniae. K. quasipneumoniae subsp. quasipneumoniae has been recovered in clinicalspecimens from patients with biliary tract infection (141), liver abscess (142), andurinary tract infection (143), while K. quasipneumoniae subsp. similipneumoniae hasbeen implicated in urinary tract infection (144), sepsis (with antecedent necrotizingfasciitis) (145), odontogenic infection (147), and nosocomial infection (148). In additionto recent reports of Acinetobacter variabilis isolation in the context of neonatal sepsis(149) and cystic fibrosis (150), organism-specific nucleic acid has been isolated fromPediculus humanus capitis organisms collected from schoolchildren and homelessindividuals in northern Africa (176, 177). The authors raise the possibility of humanbody lice potentially serving as vectors/reservoirs of a range of pathogens broader thanpreviously appreciated.
Other novel agents of interest. One taxon briefly described in the first bacterialtaxonomy compendium (1) was Klebsiella michiganensis, an isolate of which wasoriginally recovered from a toothbrush holder. In 2018, Zheng et al. (157) reported acase of acute diarrhea from a patient after hematopoietic stem cell transplantation inwhich a K. michiganensis isolate harboring the resistance determinants KPC-2, NDM-1,and NDM-5 was recovered from a stool culture (Table 3). While not included within theformal tables of this minireview, the following paragraphs describe examples of newtaxa that possess the potential to progress into the realm of human clinical disease.
Although they have yet to be associated with human clinical specimens, several newtaxa have been cultivated from known disease vector agents. These include therickettsial agents Rickettsia asembonensis sp. nov., Rickettsia amblyommatis sp. nov.,Rickettsia gravesii sp. nov., and Occidentia massiliensis gen. nov., sp. nov., recoveredfrom fleas (178) or ticks (179–181); Borrelia bissettiae sp. nov., Borrelia californiensis sp.nov., and Borrelia lanei sp. nov. from Ixodes pacificus ticks (182, 183); three novelAnaplasmataceae from ticks (184, 185); and the Gram-negative bacillus Coetzeea brasil-iensis gen. nov., sp. nov., from mosquito larvae (186). The valid O. massiliensis gen. nov.,sp. nov., designation was subsequently added by IJSEM (74).
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Other agents have been associated with ingestible or inhalable material. Serratiaaquatilis sp. nov. and Ampullimonas aquatilis gen. nov., sp. nov., have recently beenisolated from drinking (187) and bottled mineral (188) water, respectively. Agentsrecovered from raw cow’s milk include Pseudomonas helleri sp. nov., Pseudomonasweihenstephanensis sp. nov. (189), Pseudomonas lactis sp. nov., and Pseudomonasparalactis sp. nov. (190). Rooney et al. (191) reported the isolation of Acinetobacterlactucae sp. nov. from iceberg lettuce. Examples of novel agents recovered fromseafood include Halomonas garicola sp. nov. (192), Proteus cibarius sp. nov. (193), andThalassotalea crassostreae sp. nov. (194). Finally, several nonfermentative Gram-negative bacilli have been isolated from air-conditioning systems (195–199).
In summary, studies of the human microbiome and advancements in molecularcharacterization modalities have largely been responsible for the identification of novelbacterial agents from human sources. Newer and improved tools have also contributedto the assessment of closely related pathogens and, in many instances, have resultedin revisions to previously accepted taxonomy. We have attempted to summarize thesechanges for 2016 and 2017 (as relevant to humans) and to provide insight into theclinical relevance of these agents. Additional changes to the Clostridiales are anticipatedin the next few years. As a result, this project will be sustainable into the near future,while retrospectively attempting to ascertain the clinical significance of agents that arecurrently believed to have uncertain or commensal status.
ACKNOWLEDGMENTThis report was not subject to influence from any funding agency in the public,
commercial, or not-for-profit sectors.
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