supporting information reveals variability in evolutionary ... · supporting information systems...

25
Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability in evolutionary co-conservation Amphun Chaiboonchoe a† , Lila Ghamsari b† , Bushra Dohai a† , Patrick Ng c† , Basel Khraiwesh a , Ashish Jaiswal a , Kenan Jijakli a , Joseph Koussa a , David R. Nelson a , Hong Cai a§ , Xinping Yang b , Roger L. Chang d , Jason Papin e* , Haiyuan Yu c* , Santhanam Balaji a,b,f* , Kourosh Salehi-Ashtiani a,b* a Division of Science and Math, New York University Abu Dhabi and Center for Genomics and Systems Biology (CGSB), New York University Abu Dhabi Institute, Abu Dhabi, UAE b Center for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana-Farber Cancer Institute, and Department of Genetics, Harvard Medical School, Boston, MA, USA c Department of Biological Statistics and Computational Biology and Weill Institute for Cell and Molecular Biology, Cornell University, Ithaca, NY, USA d Department of Systems Biology, Harvard Medical School, Boston, MA, USA e Department of Biomedical Engineering, University of Virginia, Charlottesville, VA, USA f MRC Laboratory of Molecular Biology, Cambridge, UK. *Correspondence to: [email protected], [email protected], [email protected], [email protected] These authors contributed equally to this work § Present address: BGI-Shenzhen, Shenzhen 518083, China 1 Electronic Supplementary Material (ESI) for Molecular BioSystems. This journal is © The Royal Society of Chemistry 2016

Upload: others

Post on 14-Mar-2020

2 views

Category:

Documents


0 download

TRANSCRIPT

Page 1: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

Supporting Information

Systems level analysis of the Chlamydomonas reinhardtii metabolic network

reveals variability in evolutionary co-conservation

Amphun Chaiboonchoea†, Lila Ghamsarib†, Bushra Dohaia†, Patrick Ngc†, Basel Khraiwesha, Ashish

Jaiswala, Kenan Jijaklia, Joseph Koussaa, David R. Nelsona, Hong Caia§, Xinping Yangb, Roger L.

Changd, Jason Papine*, Haiyuan Yuc*, Santhanam Balajia,b,f*, Kourosh Salehi-Ashtiania,b*

aDivision of Science and Math, New York University Abu Dhabi and Center for Genomics and

Systems Biology (CGSB), New York University Abu Dhabi Institute, Abu Dhabi, UAE bCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana-Farber

Cancer Institute, and Department of Genetics, Harvard Medical School, Boston, MA, USAcDepartment of Biological Statistics and Computational Biology and Weill

Institute for Cell and Molecular Biology, Cornell University, Ithaca, NY, USAdDepartment of Systems Biology, Harvard Medical School, Boston, MA, USAeDepartment of Biomedical Engineering, University of Virginia, Charlottesville, VA, USAfMRC Laboratory of Molecular Biology, Cambridge, UK.

*Correspondence to: [email protected], [email protected], [email protected],

[email protected]

†These authors contributed equally to this work §Present address: BGI-Shenzhen, Shenzhen 518083, China

1

Electronic Supplementary Material (ESI) for Molecular BioSystems.This journal is © The Royal Society of Chemistry 2016

Page 2: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

Supplementary Figures: S1-S17

Fig. S1 Transformation of the Chlamydomonas Metabolic network to a gene-centric network. Conceptual transformation of a metabolic pathway (where nodes are metabolites) to a protein centric pathway (where nodes are gene products) is shown in (a), herein referred to as “type A transformation” where edges (typically enzymes) are transformed to nodes. In the resulting pathway, edges are connected to each other through metabolites. Following type A transformation of the Chlamydomonas metabolic network 1, 2, the number of connections between genes (degree) and the number of genes with the relevant degree is plotted for the resulting network in (b). The distribution suggests a non-linear trend with many genes with “few” connections and few genes with “many” connections as observed in most other biological networks like protein-protein interaction or gene regulatory networks. Currency metabolites (see Network Transformation) were excluded from the transformation.

2

Page 3: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

Fig. S2 The transformed, protein-centric metabolic network of C. reinhardtii. A graphical representation of the transformed C. reinhardtii metabolic network. Following removal of currency metabolites, the gene-reaction-metabolite associations described in the network were used to transform the genome-scale metabolic network of C. reinhardtii to a gene-centric network. There are altogether 1,081 gene products and 11,094 edges (links). This network displays a scale-free non-linear distribution between the number of genes and their connections (see Fig. S1). The colors of the nodes represent their connectivity degree (blue highest, dark-red lowest); the size of the nodes corresponds to the clustering co-efficient of the nodes; the size and color of the edges correspond to edge-betweenness (short or blue, low; long or red, high).

3

Page 4: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

Fig. S3 GO term enrichment analyses of dynamically and statically co-conserved pairs. Statistically significant GO terms for Biological Process ontology with enrichment values of p< 0.1 are shown for static (red) or dynamic (green) pairs (a). Statistically significant GO terms for Molecular Function ontology with enrichment values of p< 0.1 are shown in (b) for static (red) or dynamic (green) pairs. The bars represent the enrichment score (y-axis) of the dynamic and static in different biological functions (x-axis).

apy

rim

idin

e nu

cleo

tide

bios

ynth

etic

pro

cess

lipid

gly

cosy

latio

nL-

seri

ne m

etab

olic

pro

cess

gluc

oneo

gene

sis

cofa

ctor

met

abol

ic p

roce

sspy

rim

idin

e nu

cleo

tide

met

abol

ic p

roce

ssri

bonu

cleo

side

mon

opho

spha

te b

iosy

nthe

tic p

roce

ssri

bonu

cleo

side

mon

opho

spha

te m

etab

olic

pro

cess

bios

ynth

etic

pro

cess

cofa

ctor

bio

synt

hetic

pro

cess

grou

p tr

ansf

er co

enzy

me

met

abol

ic p

roce

ssco

enzy

me

met

abol

ic p

roce

ssnu

cleo

side

mon

opho

spha

te m

etab

olic

pro

cess

nucl

eosi

de m

onop

hosp

hate

bio

synt

hetic

pro

cess

ribo

nucl

eosi

de m

etab

olic

pro

cess

oxid

atio

n re

duct

ion

cGM

P bi

osyn

thet

ic p

roce

ssce

llula

r lip

id ca

tabo

lic p

roce

ssas

para

gine

met

abol

ic p

roce

ssas

para

gine

bio

synt

hetic

pro

cess

fatt

y ac

id b

eta-

oxid

atio

nlip

id o

xida

tion

lipid

cata

bolic

pro

cess

fatt

y ac

id ca

tabo

lic p

roce

ssfa

tty

acid

oxi

datio

ncG

MP

met

abol

ic p

roce

ss

0.00E+00 Dynamic Static

b

tran

sfer

ase

activ

ity,

tran

sfer

ring

gly

cosy

l gro

ups

gala

ctos

idas

e ac

tivity

beta

-gal

acto

sida

se a

ctiv

ityin

tram

olec

ular

oxi

dore

duct

ase

activ

ity, t

rans

posi

ng C

=Cbo

nds

vita

min

bin

ding

calc

ium

ion

bind

ing

oxid

ored

ucta

se a

ctiv

ity, a

ctin

gon

sulfu

r gro

up o

f don

ors

nucl

eotid

e ki

nase

act

ivity

carb

ohyd

rate

kin

ase

activ

ity

phos

phor

us-o

xyge

n ly

ase

activ

ityin

tram

olec

ular

tran

sfer

ase

activ

ity

cycl

ase

activ

ity

guan

ylat

e cy

clas

e ac

tivity

antio

xida

nt a

ctiv

ity

acyl

-CoA

oxi

dase

act

ivity

alph

a-am

ylas

e ac

tivity

aspa

ragi

ne sy

ntha

se(g

luta

min

e-hy

drol

yzin

g)ac

tivity

@

@

@

@

@

@ Dynamic Static

4

Page 5: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

Fig. S4 The largest five co-conserved hubs in the network. The hubs in the network were defined as nodes forming the top 20% of highly connected genes. The five most connected hubs in the network are shown: Hubs 1-4 encode ferredoxins, hub 5 encodes an acyl-carrier protein (ACP2). Green edges are between nodes showing evidence of dynamic co-conservation, red edges are between statically co-conserved pairs.

5

1

2

3 4

5

Page 6: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

Fig. S5 Gene ontology (GO) and interolog analysis of C. reinhardtii with S.cerevisiae and A.thaliana. GO terms (Biological process) of dynamically co-conserved interologs of C. reinhardtii/A. thaliana, and interologs of C. reinhardtii/S. cerevisiae are shown in (a) and (b) respectively; GO terms of statically co-conserved interlogs of C. reinhardtii/A. thaliana, and interologs of C.reinhardtii/S.cerevisiae are shown in (c) and (d). BinGO (a biological network gene ontology tool) was used to visualize the GO terms that were statistically overrepresented (hypergeometric test) in the gene sets. Nodes highlighted in yellow correspond to GO terms with a p-value of 0.05 or smaller.

6

iron

ion

tran

spor

t sodi

um io

n tr

ansp

ort

di-,

tri-

vale

nt in

orga

nic

catio

n tr

ansp

ort

tran

sitio

n m

etal

ion

tran

spor

tmet

al io

n tr

ansp

ort

catio

n tr

ansp

ort

mon

oval

ent i

norg

anic

cat

ion

tran

spor

t

phos

phat

e tr

ansp

ort

inor

gani

c an

ion

tran

spor

t

anio

n tr

ansp

ort

ion

tran

spor

t

tran

spor

t

regu

latio

n of

bio

logi

cal p

roce

ss

regu

latio

n of

cel

lula

r pro

cess

lysi

ne b

iosy

nthe

tic p

roce

ss v

ia

diam

inop

imel

ate

sign

al tr

ansm

issi

onas

para

gine

met

abol

ic p

roce

ss

lysi

ne b

iosy

nthe

tic p

roce

ss

sign

al tr

ansd

uctio

n

sign

alin

g pr

oces

sas

part

ate

fam

ily a

min

o ac

id

met

abol

ic p

roce

ss

aspa

rtat

e fa

mily

am

ino

acid

bi

osyn

thet

ic p

roce

ss

dica

rbox

ylic

aci

d m

etab

olic

pro

cess

sign

alin

g

biol

ogic

al re

gula

tion

glut

amin

e fa

mily

am

ino

acid

m

etab

olic

pro

cess

gl

utam

ine

fam

ily a

min

o ac

id

bios

ynth

etic

pro

cess

glut

amin

e m

etab

olic

pro

cess

glut

amin

e bi

osyn

thet

ic p

roce

ss

esta

blis

hmen

t of l

ocal

izat

ion

ribon

ucle

osid

e tr

ipho

spha

te

bios

ynth

etic

pro

cess

puri

ne ri

bonu

cleo

tide

bios

ynth

etic

pr

oces

s

purin

e rib

onuc

leos

ide

trip

hosp

hate

bi

osyn

thet

ic p

roce

ss

purin

e rib

onuc

leos

ide

trip

hosp

hate

m

etab

olic

pro

cess

pu

rine

nucl

eosi

de tr

ipho

spha

te

bios

ynth

etic

pro

cess

GTP

met

abol

ic p

roce

ss

GTP

bio

synt

hetic

pro

cess

puri

ne r

ibon

ucle

otid

e m

etab

olic

pr

oces

s pu

rine

nucl

eosi

de tr

ipho

spha

te

met

abol

ic p

roce

ss

ribo

nucl

eosi

de tr

ipho

spha

te

met

abol

ic p

roce

ss

purin

e nu

cleo

tide

bios

ynth

etic

pr

oces

s

nucl

eosi

de tr

ipho

spha

te

bios

ynth

etic

pro

cess

rib

onuc

leot

ide

bios

ynth

etic

pro

cess

nucl

eotid

e m

etab

olic

pro

cess

cGM

P m

etab

olic

pro

cess

nucl

eotid

e bi

osyn

thet

ic p

roce

ss

purin

e nu

cleo

tide

met

abol

ic p

roce

ss

ribon

ucle

otid

e m

etab

olic

pro

cess

nucl

eosi

de tr

ipho

spha

te m

etab

olic

pr

oces

s

nucl

eic

acid

met

abol

ic p

roce

ss

nucl

eoba

se, n

ucle

osid

e, n

ucle

otid

e an

d nu

clei

c ac

id b

iosy

nthe

tic

proc

ess

ribof

lavi

n bi

osyn

thet

ic p

roce

ss

cellu

lar p

rote

in m

etab

olic

pro

cess

cellu

lar m

acro

mol

ecul

e m

etab

olic

pr

oces

s

ribof

lavi

n m

etab

olic

pro

cess

vita

min

bio

synt

hetic

pro

cess

cellu

lar n

itrog

en c

ompo

und

bios

ynth

etic

pro

cess

nucl

eoba

se, n

ucle

osid

e, n

ucle

otid

e an

d nu

clei

c ac

id m

etab

olic

pro

cess

prot

ein

met

abol

ic p

roce

ss carb

ohyd

rate

met

abol

ic p

roce

sssm

all m

olec

ule

met

abol

ic p

roce

ss

cellu

lar c

arbo

hydr

ate

bios

ynth

etic

pr

oces

s

bios

ynth

etic

pro

cess

smal

l mol

ecul

e bi

osyn

thet

ic p

roce

ss

carb

ohyd

rate

bio

synt

hetic

pro

cess

prim

ary

met

abol

ic p

roce

ss

alco

hol m

etab

olic

pro

cess

mon

osac

char

ide

bios

ynth

etic

pr

oces

s

alco

hol b

iosy

nthe

tic p

roce

ss

smal

l mol

ecul

e ca

tabo

lic p

roce

ss

wat

er-s

olub

le v

itam

in m

etab

olic

pr

oces

s

carb

ohyd

rate

cat

abol

ic p

roce

ss

cellu

lar m

etab

olic

pro

cess

orga

nic

acid

bio

synt

hetic

pro

cess

lipid

met

abol

ic p

roce

ss

cata

bolic

pro

cess

fatty

aci

d m

etab

olic

pro

cess

oxoa

cid

met

abol

ic p

roce

ss

pyru

vate

met

abol

ic p

roce

ss

phot

osyn

thes

is, l

ight

rea

ctio

n

isop

reno

id m

etab

olic

pro

cess

cellu

lar c

arbo

hydr

ate

met

abol

ic

proc

ess

orga

nic

acid

met

abol

ic p

roce

ssce

llula

r ket

one

met

abol

ic p

roce

ss

isop

reno

id b

iosy

nthe

tic p

roce

ss

lipid

bio

synt

hetic

pro

cess

cellu

lar l

ipid

met

abol

ic p

roce

ssph

otos

ynth

esis

ribof

lavi

n an

d de

rivat

ive

met

abol

ic

proc

ess

nucl

eoba

se, n

ucle

osid

e an

d nu

cleo

tide

bios

ynth

etic

pro

cess

wat

er-s

olub

le v

itam

in b

iosy

nthe

tic

proc

ess

nucl

eoba

se, n

ucle

osid

e an

d nu

cleo

tide

met

abol

ic p

roce

ss

ribof

lavi

n an

d de

rivat

ive

bios

ynth

etic

pro

cess

vita

min

met

abol

ic p

roce

ss

phos

phor

us m

etab

olic

pro

cess

mac

rom

olec

ule

bios

ynth

etic

pro

cess

hete

rocy

cle

met

abol

ic p

roce

ss

cellu

lar n

itrog

en c

ompo

und

met

abol

ic p

roce

ss

met

abol

ic p

roce

ss

cellu

lar c

atab

olic

pro

cess

mac

rom

olec

ule

met

abol

ic p

roce

ss

cellu

lar m

acro

mol

ecul

e bi

osyn

thet

ic

proc

ess D

NA

met

abol

ic p

roce

ss

cellu

lar b

iosy

nthe

tic p

roce

ss

folic

aci

d an

d de

rivat

ive

met

abol

ic

proc

ess

thio

este

r met

abol

ic p

roce

ss

cofa

ctor

met

abol

ic p

roce

ss

cellu

lar n

itrog

en c

ompo

und

cata

bolic

pro

cess

thio

este

r bio

synt

hetic

pro

cess

folic

aci

d an

d de

rivat

ive

bios

ynth

etic

pr

oces

s

coen

zym

e m

etab

olic

pro

cess

cofa

ctor

cat

abol

ic p

roce

ss

cofa

ctor

bio

synt

hetic

pro

cess

pigm

ent m

etab

olic

pro

cess

nitr

ogen

com

poun

d m

etab

olic

pr

oces

s

grou

p tr

ansf

er c

oenz

yme

met

abol

ic

proc

ess

porp

hyrin

met

abol

ic p

roce

ss

hem

e m

etab

olic

pro

cess

acyl

-CoA

bio

synt

hetic

pro

cess

fatty

-acy

l-CoA

met

abol

ic p

roce

ss

fatty

-acy

l-CoA

bio

synt

hetic

pro

cess

hom

eost

atic

pro

cess

cellu

lar c

hem

ical

hom

eost

asis

arom

atic

com

poun

d bi

osyn

thet

ic

proc

ess

amin

e bi

osyn

thet

ic p

roce

ss

sulfu

r met

abol

ic p

roce

ss

sulfu

r com

poun

d bi

osyn

thet

ic

proc

ess

cellu

lar p

roce

ss

arom

atic

am

ino

acid

fam

ily

met

abol

ic p

roce

ss

sulfu

r am

ino

acid

met

abol

ic p

roce

sscellu

lar a

rom

atic

com

poun

d m

etab

olic

pro

cess

cellu

lar a

min

o ac

id a

nd d

eriv

ativ

e m

etab

olic

pro

cess

mon

ocar

boxy

lic a

cid

met

abol

ic

proc

ess

fatty

aci

d bi

osyn

thet

ic p

roce

ss

cellu

lar a

min

e m

etab

olic

pro

cess

amin

e m

etab

olic

pro

cess

carb

oxyl

ic a

cid

met

abol

ic p

roce

ss

diam

inop

imel

ate

met

abol

ic p

roce

ss

chor

ism

ate

met

abol

ic p

roce

ss

oxid

atio

n re

duct

ion

carb

oxyl

ic a

cid

bios

ynth

etic

pro

cess

arom

atic

am

ino

acid

fam

ily

bios

ynth

etic

pro

cess

iron

ion

hom

eost

asis

di-,

tri-

vale

nt in

orga

nic

catio

n ho

meo

stas

is

catio

n ho

meo

stas

is cellu

lar i

on h

omeo

stas

is

chem

ical

hom

eost

asis

cellu

lar c

atio

n ho

meo

stas

is

ion

hom

eost

asis

cellu

lar i

ron

ion

hom

eost

asis

cellu

lar d

i-, t

ri-v

alen

t ino

rgan

ic

catio

n ho

meo

stas

is

loca

lizat

ion

serin

e fa

mily

am

ino

acid

met

abol

ic

proc

ess

cellu

lar a

min

o ac

id b

iosy

nthe

tic

proc

ess bi

olog

ical

_pro

cess

cellu

lar a

min

o ac

id m

etab

olic

pr

oces

s L-

serin

e m

etab

olic

pro

cess

cyst

eine

bio

synt

hetic

pro

cess

from

se

rine

cyst

eine

bio

synt

hetic

pro

cess

sulfu

r am

ino

acid

bio

synt

hetic

pr

oces

s

lysi

ne m

etab

olic

pro

cess

cyst

eine

met

abol

ic p

roce

ss

regu

latio

n of

bio

logi

cal q

ualit

y

aspa

ragi

ne b

iosy

nthe

tic p

roce

ss

serin

e fa

mily

am

ino

acid

bi

osyn

thet

ic p

roce

ss

tran

smem

bran

e tr

ansp

ort

cellu

lar h

omeo

stas

is

RN

A-d

epen

dent

DN

A re

plic

atio

n

tran

slat

ion

tetr

apyr

role

met

abol

ic p

roce

ss

gene

exp

ress

ion

DN

A re

plic

atio

n

hete

rocy

cle

cata

bolic

pro

cess

hem

e ox

idat

ion

tetr

apyr

role

cat

abol

ic p

roce

ss

coen

zym

e bi

osyn

thet

ic p

roce

ss

acyl

-CoA

met

abol

ic p

roce

ss

porp

hyrin

cat

abol

ic p

roce

ss

gluc

ose

6-ph

osph

ate

met

abol

ic

proc

ess

gluc

ose

met

abol

ic p

roce

ss

gluc

ose

cata

bolic

pro

cess

mon

osac

char

ide

cata

bolic

pro

cess

hexo

se c

atab

olic

pro

cess

hexo

se m

etab

olic

pro

cess

gene

ratio

n of

pre

curs

or m

etab

olite

s an

d en

ergy

phot

osyn

thes

is, l

ight

har

vest

ing

mon

osac

char

ide

met

abol

ic p

roce

ss

gluc

oneo

gene

sis

glyc

olys

is

hexo

se b

iosy

nthe

tic p

roce

ss

cycl

ic n

ucle

otid

e bi

osyn

thet

ic

proc

ess

cycl

ic n

ucle

otid

e m

etab

olic

pro

cess

nucl

eosi

de m

onop

hosp

hate

m

etab

olic

pro

cess

nucl

eotid

e ph

osph

oryl

atio

n

phos

phor

ylat

ion

nucl

eosi

de d

ipho

spha

te m

etab

olic

pr

oces

s

nucl

eosi

de m

onop

hosp

hate

bi

osyn

thet

ic p

roce

ss

nucl

eosi

de d

ipho

spha

te

phos

phor

ylat

ion

alco

hol c

atab

olic

pro

cess

phos

phat

e m

etab

olic

pro

cess

nucl

eosi

de m

etab

olic

pro

cess

nucl

eosi

de p

hosp

hate

met

abol

ic

proc

ess

cellu

lar c

arbo

hydr

ate

cata

bolic

pr

oces

s

cGM

P bi

osyn

thet

ic p

roce

ss

a

Page 7: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

glyc

osyl

atio

n

glyc

erol

met

abol

ic p

roce

ss

carb

ohyd

rate

met

abol

ic p

roce

ss

prot

ein

met

abol

ic p

roce

ss

gene

exp

ress

ion

prim

ary

met

abol

ic p

roce

sstr

ansl

atio

n

tran

spor

t

loca

lizat

ion

gluc

ose

met

abol

ic p

roce

ss

hexo

se m

etab

olic

pro

cess

esta

blis

hmen

t of l

ocal

izat

ion

cellu

lar p

rote

in m

etab

olic

pro

cess

aldi

tol m

etab

olic

pro

cess

mac

rom

olec

ule

mod

ifica

tion

poly

ol m

etab

olic

pro

cess

prot

ein

amin

o ac

id g

lyco

syla

tion

mac

rom

olec

ule

glyc

osyl

atio

n

prot

ein

mod

ifica

tion

proc

ess

glyc

opro

tein

met

abol

ic p

roce

ss

bios

ynth

etic

pro

cess

cellu

lar m

etab

olic

pro

cess

smal

l mol

ecul

e m

etab

olic

pro

cess

cellu

lar p

roce

ss

oxid

atio

n re

duct

ion

biol

ogic

al_p

roce

ss

met

abol

ic p

roce

ss

tran

smem

bran

e tr

ansp

ort

oxoa

cid

met

abol

ic p

roce

ss

smal

l mol

ecul

e bi

osyn

thet

ic p

roce

ss

cellu

lar a

min

e m

etab

olic

pro

cess

amin

e bi

osyn

thet

ic p

roce

ss

cellu

lar a

min

o ac

id b

iosy

nthe

tic

proc

ess

cellu

lar k

eton

e m

etab

olic

pro

cess

orga

nic

acid

met

abol

ic p

roce

ss

orga

nic

acid

bio

synt

hetic

pro

cess

amin

e m

etab

olic

pro

cess

cellu

lar n

itrog

en c

ompo

und

bios

ynth

etic

pro

cess

nitr

ogen

com

poun

d m

etab

olic

pr

oces

s

cellu

lar n

itrog

en c

ompo

und

met

abol

ic p

roce

ss

cellu

lar b

iosy

nthe

tic p

roce

ss

mac

rom

olec

ule

bios

ynth

etic

pro

cess

cellu

lar a

min

o ac

id a

nd d

eriv

ativ

e m

etab

olic

pro

cess

prot

ein

amin

o ac

id N

-lin

ked

glyc

osyl

atio

n vi

a as

para

gine

pept

idyl

-asp

arag

ine

mod

ifica

tion

pept

idyl

-am

ino

acid

mod

ifica

tion

prot

ein

amin

o ac

id N

-lin

ked

glyc

osyl

atio

n

cellu

lar a

min

o ac

id m

etab

olic

pr

oces

s

carb

oxyl

ic a

cid

met

abol

ic p

roce

ss

bran

ched

cha

in fa

mily

am

ino

acid

m

etab

olic

pro

cess

carb

oxyl

ic a

cid

bios

ynth

etic

pro

cess

bran

ched

cha

in fa

mily

am

ino

acid

bi

osyn

thet

ic p

roce

ss

cellu

lar m

acro

mol

ecul

e bi

osyn

thet

ic

proc

ess

mon

osac

char

ide

met

abol

ic p

roce

ss

glyc

opro

tein

bio

synt

hetic

pro

cess

cellu

lar c

arbo

hydr

ate

met

abol

ic

proc

ess

cellu

lar m

acro

mol

ecul

e m

etab

olic

pr

oces

s

alco

hol m

etab

olic

pro

cess

mac

rom

olec

ule

met

abol

ic p

roce

ss

b

7

Page 8: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

hist

idin

e bi

osyn

thet

ic p

roce

ss

amin

e bi

osyn

thet

ic p

roce

ss

cellu

lar a

min

e m

etab

olic

pro

cess

coen

zym

e ca

tabo

lic p

roce

ss

arom

atic

com

poun

d bi

osyn

thet

ic

proc

ess

chor

ism

ate

met

abol

ic p

roce

ss

bran

ched

cha

in fa

mily

am

ino

acid

m

etab

olic

pro

cess

cyst

eine

met

abol

ic p

roce

ss

tric

arbo

xylic

aci

d cy

cle

bran

ched

cha

in fa

mily

am

ino

acid

bi

osyn

thet

ic p

roce

ss

serin

e fa

mily

am

ino

acid

bi

osyn

thet

ic p

roce

ss

L-se

rine

met

abol

ic p

roce

ss

argi

nine

met

abol

ic p

roce

ss

ener

gy d

eriv

atio

n by

oxi

datio

n of

or

gani

c co

mpo

unds

isol

euci

ne b

iosy

nthe

tic p

roce

ss

cyst

eine

bio

synt

hetic

pro

cess

from

se

rine

isol

euci

ne m

etab

olic

pro

cess

cyst

eine

bio

synt

hetic

pro

cess

cellu

lar r

espi

ratio

n

aero

bic

resp

irat

ion

tran

smem

bran

e tr

ansp

ort

gene

ratio

n of

pre

curs

or m

etab

olite

s an

d en

ergy

is

opre

noid

bio

synt

hetic

pro

cess

phos

phol

ipid

bio

synt

hetic

pro

cess

cellu

lar m

etab

olic

pro

cess

lipid

bio

synt

hetic

pro

cess

oxoa

cid

met

abol

ic p

roce

ss

fatty

aci

d bi

osyn

thet

ic p

roce

ss

cellu

lar l

ipid

met

abol

ic p

roce

ss

cellu

lar k

eton

e m

etab

olic

pro

cess

cellu

lar c

atab

olic

pro

cess

prim

ary

met

abol

ic p

roce

ss

smal

l mol

ecul

e m

etab

olic

pro

cess

cellu

lar c

arbo

hydr

ate

bios

ynth

etic

pr

oces

s

cellu

lar m

acro

mol

ecul

e bi

osyn

thet

ic

proc

ess

cellu

lar p

rote

in m

etab

olic

pro

cess

cellu

lar c

arbo

hydr

ate

met

abol

ic

proc

ess

carb

ohyd

rate

bio

synt

hetic

pro

cess

smal

l mol

ecul

e bi

osyn

thet

ic p

roce

ss

orga

nic

acid

met

abol

ic p

roce

ss

glyc

opro

tein

bio

synt

hetic

pro

cess

carb

on u

tiliz

atio

ntr

ansl

atio

n

orga

nic

subs

tanc

e m

etab

olic

pro

cess

prot

ein

amin

o ac

id g

lyco

syla

tion

mac

rom

olec

ule

met

abol

ic p

roce

ssca

rboh

ydra

te c

atab

olic

pro

cess

esta

blis

hmen

t of l

ocal

izat

ion

biol

ogic

al_p

roce

ss

mac

rom

olec

ule

glyc

osyl

atio

nm

acro

mol

ecul

e m

odifi

catio

n

prot

ein

mod

ifica

tion

proc

ess

gene

exp

ress

ion

carb

on fi

xatio

n

glyc

opro

tein

met

abol

ic p

roce

ss

phot

osyn

thes

is

lipid

met

abol

ic p

roce

ss

orga

noph

osph

ate

met

abol

ic p

roce

ss

met

abol

ic p

roce

ss oxid

atio

n re

duct

ion

prot

ein

met

abol

ic p

roce

ss

cellu

lar m

acro

mol

ecul

e m

etab

olic

pr

oces

s

pyri

mid

ine

nucl

eotid

e m

etab

olic

pr

oces

s

hexo

se b

iosy

nthe

tic p

roce

ss

nucl

eosi

de m

etab

olic

pro

cess

gluc

oneo

gene

sis

NA

D m

etab

olic

pro

cess

glyc

erol

eth

er m

etab

olic

pro

cess

prot

ein

amin

o ac

id N

-lin

ked

glyc

osyl

atio

n vi

a as

para

gine

hexo

se m

etab

olic

pro

cess

NA

D b

iosy

nthe

tic p

roce

ss gluc

ose

met

abol

ic p

roce

ss

pept

idyl

-asp

arag

ine

mod

ifica

tion

hexo

se c

atab

olic

pro

cess

NA

DP

met

abol

ic p

roce

ss

prot

ein

amin

o ac

id N

-lin

ked

glyc

osyl

atio

n

nico

tinam

ide

nucl

eotid

e m

etab

olic

pr

oces

s

pept

idyl

-am

ino

acid

mod

ifica

tion

glyc

osyl

atio

n

wat

er-s

olub

le v

itam

in m

etab

olic

pr

oces

s

mon

osac

char

ide

bios

ynth

etic

pr

oces

s

mon

osac

char

ide

met

abol

ic p

roce

ss

mon

osac

char

ide

cata

bolic

pro

cess

alco

hol b

iosy

nthe

tic p

roce

ss

alco

hol m

etab

olic

pro

cess

alco

hol c

atab

olic

pro

cess

cellu

lar c

arbo

hydr

ate

cata

bolic

pr

oces

s

orga

nic

ethe

r met

abol

ic p

roce

ss

orga

nic

acid

bio

synt

hetic

pro

cess

cellu

lar a

min

o ac

id a

nd d

eriv

ativ

e m

etab

olic

pro

cess

pter

idin

e an

d de

riva

tive

met

abol

ic

proc

ess

mon

ocar

boxy

lic a

cid

met

abol

ic

proc

ess

mol

ybdo

pter

in c

ofac

tor m

etab

olic

pr

oces

s

coen

zym

e m

etab

olic

pro

cess

folic

aci

d an

d de

riva

tive

met

abol

ic

proc

ess

cofa

ctor

bio

synt

hetic

pro

cess

hete

rocy

cle

met

abol

ic p

roce

ss

Mo-

mol

ybdo

pter

in c

ofac

tor

met

abol

ic p

roce

ss

cellu

lar n

itrog

en c

ompo

und

bios

ynth

etic

pro

cess

carb

ohyd

rate

met

abol

ic p

roce

ss

mac

rom

olec

ule

bios

ynth

etic

pro

cess

cata

bolic

pro

cess

bios

ynth

etic

pro

cess

smal

l mol

ecul

e ca

tabo

lic p

roce

ss

purin

e nu

cleo

side

met

abol

ic p

roce

ssri

bonu

cleo

side

met

abol

ic p

roce

ssnu

cleo

tide

bios

ynth

etic

pro

cess

ribo

flavi

n an

d de

riva

tive

bios

ynth

etic

pro

cess

py

rim

idin

e nu

cleo

tide

bios

ynth

etic

pr

oces

s

pyri

mid

ine

deox

yrib

onuc

leot

ide

bios

ynth

etic

pro

cess

2'-d

eoxy

ribo

nucl

eotid

e m

etab

olic

pr

oces

s

folic

aci

d an

d de

rivat

ive

bios

ynth

etic

pr

oces

s gr

oup

tran

sfer

coe

nzym

e m

etab

olic

pr

oces

s co

enzy

me

bios

ynth

etic

pro

cess

Mo-

mol

ybdo

pter

in c

ofac

tor

bios

ynth

etic

pro

cess

ox

idor

educ

tion

coen

zym

e m

etab

olic

pr

oces

s

coen

zym

e A

bios

ynth

etic

pro

cess

sulfu

r am

ino

acid

met

abol

ic p

roce

ss

arom

atic

am

ino

acid

fam

ily

bios

ynth

etic

pro

cess

sulfu

r am

ino

acid

bio

synt

hetic

pr

oces

s ac

etyl

-CoA

cat

abol

ic p

roce

ss

cellu

lar a

min

o ac

id m

etab

olic

pr

oces

s

sulfu

r com

poun

d bi

osyn

thet

ic

proc

ess

arom

atic

am

ino

acid

fam

ily

met

abol

ic p

roce

ss

dica

rbox

ylic

aci

d m

etab

olic

pro

cess

pyru

vate

met

abol

ic p

roce

ssvi

tam

in b

iosy

nthe

tic p

roce

ss

nucl

eoba

se, n

ucle

osid

e, n

ucle

otid

e an

d nu

clei

c ac

id b

iosy

nthe

tic

proc

ess

porp

hyri

n bi

osyn

thet

ic p

roce

ss

ribo

flavi

n bi

osyn

thet

ic p

roce

ss

ribo

flavi

n m

etab

olic

pro

cess

wat

er-s

olub

le v

itam

in b

iosy

nthe

tic

proc

ess

ribo

flavi

n an

d de

riva

tive

met

abol

ic

proc

ess

nucl

eoba

se, n

ucle

osid

e an

d nu

cleo

tide

bios

ynth

etic

pro

cess

nucl

eoba

se, n

ucle

osid

e an

d nu

cleo

tide

met

abol

ic p

roce

ss

pent

ose-

phos

phat

e sh

unt

nucl

eotid

e m

etab

olic

pro

cess

nucl

eosi

de d

ipho

spha

te b

iosy

nthe

tic

proc

ess

nucl

eosi

de d

ipho

spha

te m

etab

olic

pr

oces

s

deox

yrib

onuc

leot

ide

bios

ynth

etic

pr

oces

s

deox

yrib

onuc

leot

ide

met

abol

ic

proc

ess

pyri

mid

ine

nucl

eosi

de d

ipho

spha

te

bios

ynth

etic

pro

cess

deox

yrib

onuc

leos

ide

diph

osph

ate

bios

ynth

etic

pro

cess

deox

yrib

onuc

leos

ide

diph

osph

ate

met

abol

ic p

roce

ss

pyri

mid

ine

deox

yrib

onuc

leos

ide

diph

osph

ate

bios

ynth

etic

pro

cess

2'-d

eoxy

ribo

nucl

eotid

e bi

osyn

thet

ic

proc

ess

dTD

P b

iosy

nthe

tic p

roce

ss

vita

min

met

abol

ic p

roce

ssnu

cleo

base

, nuc

leos

ide,

nuc

leot

ide

and

nucl

eic

acid

met

abol

ic p

roce

ss

gluc

ose

cata

bolic

pro

cess

pros

thet

ic g

roup

met

abol

ic p

roce

ss

nitr

ogen

com

poun

d m

etab

olic

pr

oces

s

pter

idin

e an

d de

riva

tive

bios

ynth

etic

pr

oces

s

amin

e m

etab

olic

pro

cess

porp

hyri

n m

etab

olic

pro

cess

tetr

apyr

role

bio

synt

hetic

pro

cess

hist

idin

e m

etab

olic

pro

cess

hete

rocy

cle

bios

ynth

etic

pro

cess

tetr

apyr

role

met

abol

ic p

roce

ssco

fact

or m

etab

olic

pro

cess

mol

ybdo

pter

in c

ofac

tor b

iosy

nthe

tic

proc

ess

hist

idin

e fa

mily

am

ino

acid

bi

osyn

thet

ic p

roce

ss

hist

idin

e fa

mily

am

ino

acid

m

etab

olic

pro

cess

acet

yl-C

oA m

etab

olic

pro

cess

glut

amin

e fa

mily

am

ino

acid

bi

osyn

thet

ic p

roce

ss

serin

e fa

mily

am

ino

acid

met

abol

ic

proc

ess

cellu

lar a

min

o ac

id b

iosy

nthe

tic

proc

ess ar

gini

ne b

iosy

nthe

tic p

roce

ss

glut

amin

e fa

mily

am

ino

acid

m

etab

olic

pro

cess

nico

tinam

ide

nucl

eotid

e bi

osyn

thet

ic p

roce

ss

nucl

eosi

de b

isph

osph

ate

met

abol

ic

proc

ess py

ridi

ne n

ucle

otid

e m

etab

olic

pr

oces

s

puri

ne r

ibon

ucle

osid

e m

etab

olic

pr

oces

s

coen

zym

e A

met

abol

ic p

roce

ssN

AD

PH

reg

ener

atio

n

pyri

dine

nuc

leot

ide

bios

ynth

etic

pr

oces

s

carb

oxyl

ic a

cid

met

abol

ic p

roce

ss

sulfu

r met

abol

ic p

roce

ss

fatty

aci

d m

etab

olic

pro

cess

cofa

ctor

cat

abol

ic p

roce

ss

cellu

lar n

itrog

en c

ompo

und

met

abol

ic p

roce

ss

cellu

lar b

iosy

nthe

tic p

roce

ss

glyc

olys

is

cellu

lar a

rom

atic

com

poun

d m

etab

olic

pro

cess

ca

rbox

ylic

aci

d bi

osyn

thet

ic p

roce

ss

dTD

P m

etab

olic

pro

cesspy

rim

idin

e de

oxyr

ibon

ucle

osid

e di

phos

phat

e m

etab

olic

pro

cess

pyri

mid

ine

deox

yrib

onuc

leot

ide

met

abol

ic p

roce

ss

pyri

mid

ine

nucl

eosi

de d

ipho

spha

te

met

abol

ic p

roce

ss

nucl

eosi

de p

hosp

hate

met

abol

ic

proc

ess

catio

n tr

ansp

ort

mon

oval

ent i

norg

anic

cat

ion

tran

spor

t

ion

tran

spor

t

anio

n tr

ansp

ort

prot

on tr

ansp

ort

hydr

ogen

tran

spor

t

tran

spor

t

inor

gani

c an

ion

tran

spor

t

sodi

um io

n tr

ansp

ort

met

al io

n tr

ansp

ort

phos

phat

e tr

ansp

ort

cellu

lar h

omeo

stas

is

cell

redo

x ho

meo

stas

is

sign

alin

g pr

oces

s

regu

latio

n of

cel

lula

r pro

cess

regu

latio

n of

bio

logi

cal p

roce

ss

sign

alin

g

biol

ogic

al r

egul

atio

n

phos

phol

ipid

met

abol

ic p

roce

ss

isop

reno

id m

etab

olic

pro

cess

cellu

lar p

roce

ss

sign

al tr

ansd

uctio

n

sign

al tr

ansm

issi

on

regu

latio

n of

bio

logi

cal q

ualit

y

hom

eost

atic

pro

cess

loca

lizat

ion

c

8

Page 9: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

9

catio

n tr

ansp

ort

mon

oval

ent i

norg

anic

cat

ion

tran

spor

t

tran

spor

t

esta

blis

hmen

t of l

ocal

izat

ion

loca

lizat

ion

biol

ogic

al_p

roce

ss

prot

ein

amin

o ac

id N

-lin

ked

glyc

osyl

atio

n vi

a as

para

gine

prot

ein

amin

o ac

id N

-lin

ked

glyc

osyl

atio

n

cellu

lar a

ldeh

yde

met

abol

ic p

roce

ss

pept

idyl

-am

ino

acid

mod

ifica

tionpr

otei

n m

odifi

catio

n pr

oces

s

cellu

lar p

rote

in m

etab

olic

pro

cess

glyo

xyla

te c

ycle

pept

idyl

-asp

arag

ine

mod

ifica

tion

cellu

lar c

arbo

hydr

ate

met

abol

ic

proc

ess

prot

ein

amin

o ac

id g

lyco

syla

tion

cellu

lar n

itrog

en c

ompo

und

bios

ynth

etic

pro

cess

cellu

lar b

iosy

nthe

tic p

roce

ssni

trog

en c

ompo

und

met

abol

ic

proc

ess

smal

l mol

ecul

e bi

osyn

thet

ic p

roce

ss

ATP

syn

thes

is c

oupl

ed p

roto

n tr

ansp

ort

bios

ynth

etic

pro

cess

cellu

lar a

min

o ac

id a

nd d

eriv

ativ

e m

etab

olic

pro

cess

hete

rocy

cle

bios

ynth

etic

pro

cess

tetr

apyr

role

met

abol

ic p

roce

ss

smal

l mol

ecul

e m

etab

olic

pro

cess

nucl

eoba

se, n

ucle

osid

e an

d nu

cleo

tide

bios

ynth

etic

pro

cess

nucl

eosi

de b

isph

osph

ate

met

abol

ic

proc

ess

nucl

eosi

de m

etab

olic

pro

cess

tetr

apyr

role

bio

synt

hetic

pro

cess

pter

idin

e an

d de

rivat

ive

bios

ynth

etic

pr

oces

s

Mo-

mol

ybdo

pter

in c

ofac

tor

bios

ynth

etic

pro

cess

cofa

ctor

bio

synt

hetic

pro

cess

arom

atic

com

poun

d bi

osyn

thet

ic

proc

ess

pigm

ent b

iosy

nthe

tic p

roce

ss

mol

ybdo

pter

in c

ofac

tor m

etab

olic

pr

oces

s

cellu

lar a

rom

atic

com

poun

d m

etab

olic

pro

cess

cofa

ctor

met

abol

ic p

roce

ss

Mo-

mol

ybdo

pter

in c

ofac

tor

met

abol

ic p

roce

ss

pigm

ent m

etab

olic

pro

cess

pter

idin

e an

d de

riva

tive

met

abol

ic

proc

ess

mol

ybdo

pter

in c

ofac

tor b

iosy

nthe

tic

proc

ess

phos

phor

us m

etab

olic

pro

cess

gene

exp

ress

ion

mac

rom

olec

ule

met

abol

ic p

roce

ss

mac

rom

olec

ule

mod

ifica

tion

mon

ocar

boxy

lic a

cid

met

abol

ic

proc

ess

prim

ary

met

abol

ic p

roce

ss

gene

ratio

n of

pre

curs

or m

etab

olite

s an

d en

ergy

mac

rom

olec

ule

bios

ynth

etic

pro

cess

met

abol

ic p

roce

ss

cellu

lar k

eton

e m

etab

olic

pro

cess

cellu

lar m

acro

mol

ecul

e bi

osyn

thet

ic

proc

ess

phot

osyn

thes

is

mac

rom

olec

ule

glyc

osyl

atio

ngl

ycos

ylat

ion

glyc

opro

tein

bio

synt

hetic

pro

cess

glyo

xyla

te m

etab

olic

pro

cess

tran

slat

ion

cellu

lar m

acro

mol

ecul

e m

etab

olic

pr

oces

s

carb

ohyd

rate

met

abol

ic p

roce

ssgl

ycop

rote

in m

etab

olic

pro

cess

pros

thet

ic g

roup

met

abol

ic p

roce

ss

cellu

lar p

roce

ss

ion

tran

smem

bran

e tr

ansp

ort

hydr

ogen

tran

spor

t

prot

on tr

ansp

ort

tran

smem

bran

e tr

ansp

ort

ener

gy c

oupl

ed p

roto

n tr

ansp

ort,

dow

n el

ectr

oche

mic

al g

radi

ent

oxid

atio

n re

duct

ion

ion

tran

spor

t

coen

zym

e bi

osyn

thet

ic p

roce

ss

coen

zym

e m

etab

olic

pro

cess

chlo

roph

yll m

etab

olic

pro

cess

grou

p tr

ansf

er c

oenz

yme

met

abol

ic

proc

ess

coen

zym

e A

bios

ynth

etic

pro

cess

purin

e rib

onuc

leos

ide

met

abol

ic

proc

ess

coen

zym

e A

met

abol

ic p

roce

ss

ribon

ucle

osid

e m

etab

olic

pro

cess

puri

ne n

ucle

osid

e m

etab

olic

pro

cess

porp

hyri

n bi

osyn

thet

ic p

roce

ss

chlo

roph

yll b

iosy

nthe

tic p

roce

sspo

rphy

rin

met

abol

ic p

roce

ss

cellu

lar m

etab

olic

pro

cess

nucl

eoba

se, n

ucle

osid

e, n

ucle

otid

e an

d nu

clei

c ac

id m

etab

olic

pro

cess

nu

cleo

base

, nuc

leos

ide,

nuc

leot

ide

and

nucl

eic

acid

bio

synt

hetic

pr

oces

s

nucl

eoba

se, n

ucle

osid

e an

d nu

cleo

tide

met

abol

ic p

roce

ss

hete

rocy

cle

met

abol

ic p

roce

ss

prot

ein

met

abol

ic p

roce

ss

phos

phat

e m

etab

olic

pro

cess

phos

phor

ylat

ion

oxoa

cid

met

abol

ic p

roce

ssox

idat

ive

phos

phor

ylat

ion

carb

oxyl

ic a

cid

met

abol

ic p

roce

ss

cellu

lar n

itrog

en c

ompo

und

met

abol

ic p

roce

ss

amin

e m

etab

olic

pro

cess

orga

nic

acid

bio

synt

hetic

pro

cess

amin

e bi

osyn

thet

ic p

roce

ss

cellu

lar a

min

e m

etab

olic

pro

cess

hist

idin

e fa

mily

am

ino

acid

m

etab

olic

pro

cess

carb

oxyl

ic a

cid

bios

ynth

etic

pro

cess

cellu

lar a

min

o ac

id m

etab

olic

pr

oces

s ce

llula

r am

ino

acid

bio

synt

hetic

pr

oces

s

orga

nic

acid

met

abol

ic p

roce

ss

hist

idin

e bi

osyn

thet

ic p

roce

ss

ATP

bios

ynth

etic

pro

cess

hist

idin

e m

etab

olic

pro

cess

hist

idin

e fa

mily

am

ino

acid

bi

osyn

thet

ic p

roce

ss

isol

euci

ne b

iosy

nthe

tic p

roce

ss

bran

ched

cha

in fa

mily

am

ino

acid

bi

osyn

thet

ic p

roce

ss

isol

euci

ne m

etab

olic

pro

cess

bran

ched

cha

in fa

mily

am

ino

acid

m

etab

olic

pro

cess

nucl

eosi

de tr

ipho

spha

te m

etab

olic

pr

oces

s pu

rine

nuc

leot

ide

bios

ynth

etic

pr

oces

s pu

rine

rib

onuc

leot

ide

bios

ynth

etic

pr

oces

s

puri

ne n

ucle

otid

e m

etab

olic

pro

cess

puri

ne n

ucle

osid

e tr

ipho

spha

te

met

abol

ic p

roce

ss

ribon

ucle

otid

e m

etab

olic

pro

cess

puri

ne r

ibon

ucle

otid

e m

etab

olic

pr

oces

s nu

cleo

side

pho

spha

te m

etab

olic

pr

oces

s

puri

ne r

ibon

ucle

osid

e tr

ipho

spha

te

bios

ynth

etic

pro

cess

purin

e ri

bonu

cleo

side

trip

hosp

hate

m

etab

olic

pro

cess

nucl

eotid

e m

etab

olic

pro

cess

nucl

eosi

de tr

ipho

spha

te

bios

ynth

etic

pro

cess

ribo

nucl

eotid

e bi

osyn

thet

ic p

roce

ss

ribo

nucl

eosi

de tr

ipho

spha

te

met

abol

ic p

roce

ss

puri

ne n

ucle

osid

e tr

ipho

spha

te

bios

ynth

etic

pro

cess

nucl

eotid

e bi

osyn

thet

ic p

roce

ss

deox

yrib

onuc

leot

ide

met

abol

ic

proc

ess

pyri

mid

ine

nucl

eotid

e m

etab

olic

pr

oces

s

ribo

nucl

eosi

de tr

ipho

spha

te

bios

ynth

etic

pro

cess

AT

P m

etab

olic

pro

cess

nucl

eosi

de d

ipho

spha

te m

etab

olic

pr

oces

s

pyri

mid

ine

deox

yrib

onuc

leot

ide

met

abol

ic p

roce

ss

pyri

mid

ine

nucl

eotid

e bi

osyn

thet

ic

proc

ess

pyri

mid

ine

nucl

eosi

de d

ipho

spha

te

met

abol

ic p

roce

ss

nucl

eosi

de d

ipho

spha

te b

iosy

nthe

tic

proc

ess

dTD

P bi

osyn

thet

ic p

roce

ss

deox

yrib

onuc

leos

ide

diph

osph

ate

met

abol

ic p

roce

ss

pyri

mid

ine

deox

yrib

onuc

leos

ide

diph

osph

ate

bios

ynth

etic

pro

cess

deox

yrib

onuc

leos

ide

diph

osph

ate

bios

ynth

etic

pro

cess

2'-d

eoxy

ribo

nucl

eotid

e m

etab

olic

pr

oces

s

deox

yrib

onuc

leot

ide

bios

ynth

etic

pr

oces

s

pyrim

idin

e nu

cleo

side

dip

hosp

hate

bi

osyn

thet

ic p

roce

ss

pyri

mid

ine

deox

yrib

onuc

leos

ide

diph

osph

ate

met

abol

ic p

roce

ss

pyri

mid

ine

deox

yrib

onuc

leot

ide

bios

ynth

etic

pro

cess

2'-d

eoxy

ribo

nucl

eotid

e bi

osyn

thet

ic

proc

ess

dTD

P m

etab

olic

pro

cess

d

Page 10: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

Fig. S6 Network module analysis using MCODE. The top 5 modules identified based on MCODE scores are represented from (a) 21 total modules for statically co-conserved gene pairs and (b) 41 total modules of dynamically co-conserved gene pairs. The regions of the dynamic and static sub networks where these modules were detected (Fig. 2 in the main text) can be found based on the numbers associated with each module.

10

21 3

4 5

a

b

1

2

3 4 5

1

Page 11: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

Fig. S7 Light and dark expressed genes (a) and interactions (b). Dark and light expressed genes have differential topological and functional characteristics in the network.

Fig. S8 Predicted flux values from the in silico Chlamydomonas model. Flux balance analyses were carried out for maximization of biomass under dark with acetate (blue bars) and light without acetate (red bars) conditions. Biomass yield is given on the y-axis.

1ACP

Cth

COAt

hGL

YC3P

thN

ADPt

hTS

ULth

H2t

iPE

1829

Z12Z

1835

Z9Z1

2Zt

NAD

PHtf

ALAN

A1tx

5MTA

tmDG

TPtm

MAL

AKGt

mPT

RCtm

iN

H4t

nAS

POm

G5DH

xDH

DHGP

PSEC

OAH

8AL

AAT

LUTH

CYSD

O3H

AD10

0AC

P161

9ZD9

DSFA

80AC

PHi

AACP

S1FA

COAL

160

FOLD

3GR

GTPR

DPAR

hAC

OADA

GAT1

8018

19Z1

8111

...AC

PT16

0181

11Z

ASQD

PADS

1829

Z12Z

160

DGDG

D4DS

1839

Z12Z

15Z1

64...

DGDG

W3D

S183

9Z12

Z15Z

164.

..DG

TSDS

1839

Z12Z

15Z1

835Z

...M

GDGS

1819

Z161

9ZPA

PA18

111Z

1819

ZhPL

DAGA

T160

1819

Z181

11Z1

PLDA

GAT1

8111

Z181

9Z18

11...

SQDG

S160

TAGA

H18

111Z

1811

1Z18

45Z.

..1A

GPEA

T180

1835

Z9Z1

2ZLP

LPS1

AGPE

1829

Z12Z

PLPS

A218

29Z1

2Z18

35Z9

Z1...

HSK

GAPD

Hf

PGK

GDPM

TIB

PHDH

DPS

AMCL

MM

2N

ODOy

PROA

KGOX

1AP

CPT

RBK

TRPS

2hCH

LASG

MPM

ECY3

HPH

LmAG

POP

ATPP

Hm

GTPO

PmPR

FGS

ATUD

mDU

RIK1

UTUP

PFLA

CTm

AUN

OR3D

SPH

RST

ARCH

300D

EGRA

ICDH

hrIM

DHT(

3c2h

mp)

MH

GS

-15-10

-505

101520253035

mill

imol

es g

ram

[dry

wei

ght]

-1 h

our

-1

11

Page 12: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

Fig. S9 Metabolic locations for correlated downregulation (a) and upregulation (b) of flux and gene expression levels. Numbers correspond to the number of genes expressed in each of the subcellular compartments for each set.

b

a

1

1

8

13

3470

115

1

25

8

26

28

5

55

1

1

12

Page 13: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

Fig. S10 Distribution of synthetic interactions with respect to their severity and growth condition. Synthetic interactions were identified under growth in dark with acetate (DA) and light with no acetate (LNA), the identified interactions were then binned based on the extent that biomass is reduced (in comparison to the wild-type model).

Lethal (100-80)% (60-80)% (40-20)% (20-0)%0

100

200

300

400

500

600 DA LNA

Synthetic Interactions

Num

ber

of In

tera

ctio

ns

13

Page 14: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

Fig. S11 Subnetworks of synthetic lethal interactions under dark with acetate (a) and light with out acetate (b). Synthetic lethal pairs were used to generate the shown subnetworks. The blue box represents Carbohydrate metabolic process (GO: biological process) and N-Glycan Biosynthesis (KEGG pathway). The green circle represents Electron transport (GO: biological process) and Valine, leucine and isoleucine degradation (KEGG pathway).

14

Page 15: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

Fig. S12 KEGG term enrichment between two conditions (light and dark) for synthetic lethal interactions. The bars represent the enrichment score (y-axis) of the dark with acetate (red) and light with no acetate (blue) in different KEGG pathways (x-axis).

Valin

e, le

ucin

e an

dis

oleu

cine

deg

rada

tion

Prop

anoa

te m

etab

olis

mBi

osyn

thes

is o

fal

kalo

ids d

eriv

ed fr

omor

nith

ine,

lysi

ne a

ndni

cotin

ic a

cid

Bios

ynth

esis

of

alka

loid

s der

ived

from

shik

imat

e pa

thw

ayBi

osyn

thes

is o

fal

kalo

ids d

eriv

ed fr

omhi

stid

ine

and

puri

neBi

osyn

thes

is o

f pla

ntho

rmon

esN

-Gly

can

bios

ynth

esis

Bios

ynth

esis

of

terp

enoi

ds a

nd st

eroi

dsBi

osyn

thes

is o

fal

kalo

ids d

eriv

ed fr

omte

rpen

oid

and

poly

ketid

eBi

osyn

thes

is o

fph

enyl

prop

anoi

dsPy

ruva

te m

etab

olis

mBe

nzoa

te d

egra

datio

nvi

a Co

A lig

atio

nGl

ycin

e, se

rine

and

thre

onin

e m

etab

olis

mFa

tty

acid

met

abol

ism

Buta

noat

e m

etab

olis

mTr

ypto

phan

met

abol

ism

Capr

olac

tam

degr

adat

ion

Amin

o su

gar a

ndnu

cleo

tide

suga

rm

etab

olis

mGl

utat

hion

e m

etab

olis

mPe

ntos

e an

dgl

ucur

onat

ein

terc

onve

rsio

nsGl

ycol

ysis

/Gl

ucon

eoge

nesi

sLy

sine

deg

rada

tion

Asco

rbat

e an

d al

dara

tem

etab

olis

mCy

stei

ne a

ndm

ethi

onin

e m

etab

olis

mPo

rphy

rin

and

chlo

roph

yll m

etab

olis

mDr

ug m

etab

olis

m -

othe

r enz

ymes

Pent

ose

phos

phat

epa

thw

ayPy

rim

idin

e m

etab

olis

mLi

popo

lysa

ccha

ride

bios

ynth

esis

Carb

on fi

xatio

n in

phot

osyn

thet

icor

gani

sms

Sulfu

r met

abol

ism

0.00E+00

2.00E-02

4.00E-02

6.00E-02

8.00E-02

Light with no acetate Dark with acetate

Enri

chm

ent s

core

s (L

og s

cale

)

Fig. S13 The pathways of the reactions of co-set1 in set 4 that has zero average profile distance (Table S18) in purine metabolism. The figure shows the purine metabolism as obtained from KEGG. The reactions XNDH (via xanthine dehydrogenase) and URO (via urate oxidase) are highlighted in red rectangular indicated with numbers 1 and 2, respectively. In XNDH xanthine dehydrogenase dehydrogenases the xanthine into Urate, in which the latter is oxidized into 5-Hydroxyisourate in the reaction URO.

1 2

1 XNDH 2 URO

Purine metabolism

15

Page 16: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

Fig. S14 The pathways in the n-glycan biosynthesis from KEGG of reactions in co-set5 in set 2, reactions of co-set4 set 1, and the reactions associated with lethal gene pair CRv4_Au5.s16.g6321.t1 and CRv4_Au5.s12.g3687.t1 with average profile distance 3.6 with average profile distance of 3.2,1.5 and 3.6, respectively. In this figure the red rectangles, indicated with number 2,6, and 7, correspond to reactions of co-set5 in set 2 (Suppl. Data Table S18), where the reaction DOLPTG1 is catalyzed via glycotransferase to activate a nucleotide sugar and converts it into a nucleophillic glycosyl acceptor. The reactions of GLNACT (via N-acetylglucosaminyltransferase) and G12MT2 (via ALG11 mannosyltransferase with a DXD motif) produce the sequon Asn-X-Ser/Thr through DOLPTG1 (via glycosyltransferase). The blue rectangles, indicated with numbers 2,4, and 5, correspond to reactions of co-set4 in set 1 (Suppl. Data Table S17), where both GLNACT and DOLPMT (via dolichyl-phosphate beta-D-mannosyltransferase) are needed as precursor reactions for the production of the Asn-X-Ser/Thr sequon through DOLPMT2 (via dolichyl-phosphate-mannose-glycolipid alpha-mannosyltransferase).The pink rectangles, indicated with numbers 1 and 3, correspond to the reactions associated with the lethal gene pair CRv4_Au5.s16.g6321.t1 and CRv4_Au5.s12.g3687 (Suppl. Data Table S12).CRv4_Au5.s16.g6321.t1 associates the reaction GLNACPT (via UDP-GlcNAc:dolichyl-phosphate N-acetylglucosaminephosphotransferase) in purine metabolism) and CRv4_Au5.s12.g3687.t1 associates the reaction AGAKI (via D-xylose isomerase in the fructose and mannose metabolism). The metabolisms in which both genes are involved are related through the production of mannose-GDP.

12

3 4

5

6

7

1 GLCNACPT 2 GLNACT 3 AGAKI 4 DOLPMT 5 DOLPMT2 6 G12MT2 7 DOLPGT1

N-Glycan biosynthesis

16

Page 17: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

Fig. S15 The pathways of the reactions of co-set1 in set 6 that has 3.2 average profile distance (Table S17) in fatty acid biosynthesis. The figure shows the pathways of the fatty acid biosynthesis as obtained from KEGG. The red rectangles correspond to the reaction 3OAR40 and the reaction 3HAD120, indicated with numbers 1 and 2, respectively. In this biosynthesis, 3HAD120 produces dodecanoic acid through the enzyme (3R)-3-Hydroxybutanoyl-[acyl-carrier-protein] hydro-lyase, and 3OAR40 produces the Butyryl-acp through 3-oxoacyl-[acyl-carrier-protein] reductase (n-C4:0).

17

Fatty acid biosynthesis

1

2

1 3OAR40 2 3HAD120

Page 18: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

Fig. S16 The pathways of the reactions associated with lethal gene pair CRv4_Au5.s16.g6244.t1 and CRv4_Au5.s17.g7556.t1 (Table S12), that has zero average profile distance. In this figure, the red rectangles show the reactions associated with the genes CRv4_Au5.s16.g6244 (indicated with number 1) and CRv4_Au5.s17.g7556.t1 (indicated with number 2) in steroid biosynthesis and pentose phosphate pathway, respectively, as obtained from KEGG. The gene CRv4_Au5.s17.g7556.t1 is used to catalyze the reaction glucose-6-phosphate-1-dehydrogenase (g6p-A) which converts D-Glucose 6-phophate into D-Glucono-1,5-lactone 6-phosphate in the pentose phosphate pathway. The other gene, CRv4_Au5.s16.g6244.t1, is used in steroids biosynthesis.

18

1

Steroid biosynthesis

1 CRv4_Au5.s16.g6244.t1 2 CRv4_Au5.s17.g7556.t1

2

Pentose Phosphate pathway

Page 19: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

Fig. S17 The pathways of the reactions associated with lethal gene pair CRv4_Au5.s16.g6244.t1 and CRv4_Au5.s17.g7556.t1 (Table S13) that has 3.4 average profile distance. In this figure the red rectangles show reactions associated with lethal gene CRv4_Au5.s9.g15712.t1 (indicated with number 1) and CRv4_Au5.s10.g816.t1 (indicated with number 2) that are utilized in the Glycine, Serine and Threonine metabolism and Glyoxylate and Dicarboxylate metabolism, respectively obtained from KEGG. In the glycine, serine and threonine metabolism, the glycine is converted into L-serine by the reaction glycine hydroxymethyltransferase, specifically associated with CRv4_Au5.s9.g15712.t1 gene. CRv4_Au5.s10.g816.t1 is associated with glycine synthase for the conversion of glycine into ammonia in the glyoxylate and dicarboxylate metabolism

19

1

Glycine, Serine, and Threonine metabolism Glyoxylate and Dicarboxylate metabolism

2

1 CRv4_Au5.s9.g15712.t1 2 CRv4_Au5.s10.g816.t1

Page 20: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

Supplementary Methods: S1-S6

Method S1: Evolutionary affinity assignments. BLASTP searches were done for each protein

sequence of each gene in the network against proteomes of available and completely sequenced

eukaryotic genomes. These proteome sequences were obtained from SUPERFAMILY database

(version: genome_sequence_29-Aug-2010.sql). The top ten hits for each genome (e-value cutoff 0.001)

were identified and BLASTCLUST

(http://www.ncbi.nlm.nih.gov/IEB/ToolBox/C_DOC/lxr/source/doc/blast/blastclust.html) was done on

these hits to identify homology clusters (sequence identity of 30% and length cut-off of 70%) 3. Each

genome was further categorized into one of the thirteen eukaryotic lineages. Evolutionary conservation

of C. reinhardtii genes was defined on the basis of lineages present in each cluster was identified by

BLASTCLUST. Using this approach, each metabolic gene in the network was determined to be

conserved/non-conserved in each of the major eukaryotic lineages e.g., fungi, animals, plants, etc.

Method S2: Co-conservation analyses. Mutual information index (MI) and evolutionary profile

distance (PD) calculations – Mutual information index 4 for neighboring gene pairs X, Y, were

calculated as follows:

MI (X, Y) = H(X)+H(Y)-H(X,Y)

Where H(N) = Σ(-(frequency of affinity index)*log(frequency of affinity index)); H(X,Y) is the frequency

of co-occurrence affinity index and affinity index values are 0 or 1.

Evolutionary profile distance (PD) was obtained by measuring Euclidean distance between each

neighboring gene in the real or randomized network as follows:

PD (X, Y) = √ (Σ over N’s (value of lineage N of Gene1 – Value of Lineage N of Gene 2)^2), where N =

1 to 13). This definition is a variant of profile similarity used for gene expression clustering and

analysis5.

Profile randomization – For the randomization processes, the phylogenetic profile for each gene is

randomized such that the binary affinity values of “1” and “0” were retained but their positional

occurrences were varied. Thus the generated randomized phylogenetic profiles evaluated MI and PD

values for each pair of genes in the network. We note that for these analyses, the positions of genes in

the network were not randomized to evaluate the significance as evolution information content comes

from phylogenetic profiles.

Network randomization and p-value calculations - For the MI and PD calculations, significant p-values

were estimated by using random networks. These random networks were generated from the original

network by maintaining the number of partners per gene while rewiring randomly their partners. We

generated 1,000 such random networks and for every pair of genes in each network we calculated MI

and PD values then performed randomization of profiles as described (above) and evaluated how often

20

Page 21: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

the difference in the trend between randomized profiles and original profiles for these random networks

was found to be equal or higher for the real network.

Method S3: Statistical analysis of synthetic interactions-Kolmogrov-Smirnov test. To check the

normality of the profile distance distribution within the synthetically interacting gene sets, we

performed a Kolmogorov-Smirnov (KS) test measuring the maximum absolute difference between our

data and standard normal distribution. The standard normal distribution was obtained from profile

distances between all the 1,086 genes in the network. The KS test determines if the null hypothesis, that

the data comes from a standard normal distribution, or the alternative, that it does not come from such a

distribution, applies. A result of h = 1 is returned if the test rejects the null hypothesis or 0 otherwise.

The decision is transformed into a significance level (p-value) directly compared to a chosen threshold,

5%; if p-value was less than 5%, then the difference is significant, otherwise it is not considered. As

illustrated in Table S11, the KS test revealed that the synthetic interactions distribution does not come

from a standard normal distribution. A significant difference was observed between the random pairs in

the network and the synthetic interactions profile distances at both conditions. These results show that

the evolutionary affinities of the genes involved in the synthetic interactions at both conditions LNA

and DA differ from overall pairwise distance distributions of the network.

Method S4: Statistical analysis of synthetic interactions and co-sets-Hypergeometric test. In our

analysis we performed a hypergeometric test on the profile distance data of the synthetic interactions

genes. Three success values were chosen; greater or equal to 1, greater or equal to 2, and greater or

equal to 3 for both conditions. The reason behind these choices is that most of the profile distance

values lie above 1. The test provides a statistical measure to examine if the synthetic interaction

distances are enriched for larger than random network values or not. As illustrated in Table S15,

probabilities at dark conditions were higher than those at light condition in most cases. Similarly,

statistically significant enrichment was observed in co-sets (see main text for details of these

enrichment analyses).

Method S5: Transformed metabolic networks and paired-ortholog analyses. To examine if the

found dynamic and static pairs occur in Arabidopsis and yeast networks. The latest version of a yeast

metabolic network (http://sourceforge.net/projects/yeast/files/yeast_7.11.zip) was used to generate a

gene-centric network. The yeast gene-centric network consisted of 117,559 edges (connections)

between 903 metabolic gene products, with an average connectivity of ~260, and clustering coefficient

of 0.83. The network has 2 connected components. We transformed the Arabidopsis metabolic network,

reported by Mintz-oron et al., 2011, which consisted of 1,363 unique reactions and 1,078 metabolites 6.

The Arabidopsis gene-centric network consisted of 369,479 edges (connections) between 1,792

metabolic gene products with an average connectivity of ~73, and clustering coefficient of 0.50. The

network has 5 connected components.

21

Page 22: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

The ortholog annotation of genes from multiple genomes between C. reinhardtii, A. thalina and S.

cerevisiae were derived from the 11th version of OMA (Orthologus Matrix) Database7

(http://omabrawer.org). The Chlamydomonas IDs are from mapping of Augustus 5 (with BLAST) to

Phytozome version 8 (http://www.phytozome.net/).

Gene ontology analysis was used to identify enrichment, the conservation or rewiring of functional

categories of the orthologue genes that had a common ancestor between C. reinhardtii to A. thalina and

S. cerevisiae. The entire interologs static and dynamic pairs found between C. reinhardtii/S. cerevisiae

and C. reinhardtii/A. thalina were used to examine the functional categories. We identified the multiple

GO enriched functional categories that conserved and varied between the three model organisms as

shown in Figure 4 and Figure S5 A-D. Over-representation of GO terms in a set of genes was

determined by using the Biological Networks Gene Ontology tool (BiNGO)

(http://ww.psb.ugent.be/cbd/papers/BiNGO/) 8. BiNGO retrieved the relevant GO annotation then tested

for significance using the Hypergeometric test with no corrected for multiple testing. Statistically,

hypergeometric distribution is a measure of the probability that describes the number of successes in a

sequence of n draws from a finite population without replacement. GO categories that were

significantly over-represented among the differentially expressed proteins were identified.

Method S6: Correlated and anti-correlated analyses of expression and flux. The crosstalk between

metabolic reactions and gene regulation are essential and fundamental to the living cell. The cell adjusts

gene regulatory network and shifts metabolic phenotypic states according to environmental changes. In

this segment, differential expression of mRNA under two conditions (dark with acetate and light

without acetate) was compared with metabolic flux levels based on the reactions as shown in Figure S8.

The reactions were optimized for biomass production under the corresponding light (no acetate) and

dark with acetate growth conditions. We considered the collective expression of all genes in reactions

rather than individual genes; we computed the total expression levels of all genes from dark (with

acetate) to light (without acetate) conditions.

The expression patterns and regulation of a number of enzymes that catalyze the same reaction are often

different 9. To explore the agreement between changes of gene expression and predicted fluxes under

light or dark conditions, we compared these results to the reaction’s predicted fluxes by flux balance

analysis (FBA) to demonstrate the concordances of transcriptional and flux changes (Fig. S8). We

further characterized these agreements based on the compartments that the reactions occur (Fig. S9).

22

Page 23: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

Supplementary Notes: S1 and S2

Note S1: Co-sets examples for dark and light conditions. Based on Figure 6, co-set1 in set 4 (Table

S18) can be extracted as an example of a co-set with an average profile distance of 0, which signifies

that the genes associated with the co-set have similar profile distances. The reactions in this co-set,

namely URO (via urate oxidase) and XNDH (via xanthine dehydrogenase) were found to be conserved

in Amoebazoa, Fungi, Metazoa, Stramenopiles, and Verdiplantae, and they are involved in purine

metabolism. Specifically, in XNDH, the xanthine dehydrogenase dehydrogenases the xanthine into

Urate, which is oxidized into 5-Hyroxyisourate by urate oxidase and the URO reaction. In C.

reinhardtii, a urate oxidase type II enzyme was found to be activated early in response to nitrogen

starvation 10. Generally however, URO involves the oxidation of uric acid to form allantoin 11, and

XNDH involves the oxidation of hypoxanthine to xanthine and xanthine to uric acid during purine

catabolism 12 (Fig. S13).

On the other hand, co-set 5 in set 2 (Table S18) serves as an example of a co-set with a long average

profile distance (average distance of co-set 5 is 3.2). Although the genes of this co-set differ

evolutionarily due to their long profile distance, their reactions share the same biological function;

which is N-glycan biosynthesis (DOLPGT1, GLCNACT, G12MT2) with the exception of

(DM_asnglcnacglcnacman-LPAREN-man-RPAREN-man) being a demand reaction. In the n-glycan

biosynthesis, the first step is the transferase reaction of Uridine diphosphate N-acetylglucosamine and

the lipid P-Dol (dolichol phosphate) to generate a protein bound N-glycan in the cytoplasmic side of

the endoplasmic reticulum’s (ER’s) membrane. This precursor is modified by a series of reactions in

the ER and the Golgi, starting with its catalysis by glycotransferase (DOLPTG1) to activate a

nucleotide sugar and converts it into a nucleophillic glycosyl acceptor. This ensures proper folding of

the nascent protein through enabling its interaction with ER-resident chaperones, such as calnexin and

calreticulin. The reactions of GLNACT (N-acetylglucosaminyltransferase) and G12MT2 (via ALG11

mannosyltransferase with a DXD motif) produce the sequon Asn-X-Ser/Thr through DOLPTG1

(glycosyltransferase). Found in many glycosyltransferases that utilize nucleotide sugars, the DXD

motif is thought to be involved in the binding of a manganese ion that is required for association of the

enzymes with nucleotide sugar substrates. GLCNACT is associated with the CRv4_Au5.s13.g4777.t1

or CRv4_Au5.s16.g6452.t1 genes, and G12MT2 is associated with CRv4_Au5.s14.g5384.t1 (glycosyl

transferase). DOLPGT1, and GLCNACT are conserved in all 13 linages except Aloveolata and

Choanoflgellida, while the G12MT2 is not conserved in any of the 13 lineages (Fig. S14).

The genes associated with coupled reactions of co-set4 of set 1 have a low profile distance (1.5), which

means that they differ slightly in terms of evolutionary affinities. Their genes were conserved in all 13

eukaryotic lineages except Amoebozoa and Euglenzoa. The reactions of this co-set are DOLPMT2

(dolichyl-phosphate-mannose-glycolipid-alpha-mannosyltransferase), GLCNACT, and DOLPMT, and

they are also involved in the N-Glycan biosynthesis pathway, the same pathway as the previous

23

Page 24: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

example. Both GLNACT and DOLPMT are needed as precursor reactions for the production of the

Asn-X-Ser/Thr sequon through DOLPMT2 (Fig. S14).

An average profile distance of 3.2 was found between genes associated with reactions of co-set 1 in set

6 (Table S17). The coupled reactions 3HAD120 and 3OAR40 are involved in fatty acid biosynthesis

(Fig. S14). Where 3HAD120 produces dodecanoic acid through the enzyme (3R)-3-Hydroxybutanoyl-

[acyl-carrier-protein] hydro-lyase, and 3OAR40 produces the Butyryl-acp through 3-oxoacyl-[acyl-

carrier-protein] reductase (n-C4:0). The reaction 3HAD120 is associated with seven genes; five of

them are conserved in Ameobazoa, Heptophceae, and Viridiplantae. The 3OAR40 reaction is carried

out through the same seven genes with the addition of CRv4_Au5.s3.g10590.t1.

CRv4_Au5.s3.g10590.t1 is conserved in Rhodophyta and Stramenopiles and codes for an enzyme that

resembles an enoyl reductase, which catalyzes the second reduction step in fatty acid synthesis. This

enzyme is also predicted to belong to the SDRs family of diverse oxidoreductases that have a single

domain with structurally conserved Rossmann fold (alpha/beta folding pattern with a central beta-

sheet) NAD(P)(H) binding region and a structurally diverse C-terminal region.

Note S2: Synthetic interactions examples for light and dark conditions. From Fig. 6, the largest

profile distance was 3.6 and the shortest profile distance was zero. Both values exist frequently in lethal

interactions and synthetic sick interactions (80% to 100 % growth reduction).

The longest profile distance in a lethally interacting pair and under light condition was found to be 3.6.

This value is because one of the genes is conserved in all lineages while the other is not conserved in

any of the 13 eukaryotic lineages. For example the gene CRv4_Au5.s16.g6321.t1 is conserved in all

lineages while CRv4_Au5.s12.g3687.t1 is not conserved in any of the lineages. From biological aspect,

CRv4_Au5.s16.g6321.t1 is involved in the N-glycan metabolism through the UDP-GlcNAc:dolichyl-

phosphate N-acetylglucosaminephosphotransferase reaction, while the other gene

(CRv4_Au5.s12.g3687.t1) is utilized in the fructose and mannose metabolism as D-xylose isomerase.

The metabolisms in which both genes are involved are related through the production of mannose-GDP

(Fig. S14).

In contrast, the shortest profile distance among the lethal gene pairs was zero. When the profile

distance is zero, the evolutionary profile of the involved genes is the same. This means they are both

either conserved in same lineages or are both conserved in none of the thirteen eukaryotic lineages. For

example CRv4_Au5.s17.g7556.t1 (glucose-6-phosphate-1 dehydrogenase) and

CRv4_Au5.s16.g6244.t1 (cytochrome P450) are conserved in none of the thirteen lineages and are

utilized in the Pentose phosphate pathway and the Biosynthesis of steroids respectively. The gene

CRv4_Au5.s17.g7556.t1 is used to catalyze the reaction glucose-6-phosphate-1-dehydrogenase (g6p-

A) which converts D-Glucose 6-phophate into D-Glucono-1,5-lactone 6-phosphate in the pentose

phosphate pathway. The other gene, CRv4_Au5.s16.g6244.t1, is used in steroids biosynthesis

specifically for the oxidation of calcidiol into calcitriol (Fig. S16).

24

Page 25: Supporting Information reveals variability in evolutionary ... · Supporting Information Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability

Under dark growth, the lethal gene pair, CRv4_Au5.s9.g15712.t1 and CRv4_Au5.s10.g816.t1, has a

large profile distance value of 3.4. The first gene is conserved in all lineages while other one is not

conserved in any other lineages. Biologically, CRv4_Au5.s9.g15712.t1 is involved in glycine, serine

and threonine metabolism, while CRv4_Au5.s10.g816.t1 is involved in Nitrogen metabolism. In the

glycine, serine and threonine metabolism, the glycine is converted into L-serine by the reaction glycine

hydroxymethyltransferase, specifically associated with C Rv4_Au5.s9.g15712.t1 gene.

CRv4_Au5.s10.g816.t1 is associated with glycine synthase for the conversion of glycine into ammonia

in the nitrogen metabolism (Fig. S17).

References

1. R. L. Chang, L. Ghamsari, A. Manichaikul, E. F. Hom, S. Balaji, W. Fu, Y. Shen, T. Hao, B. O. Palsson, K. Salehi-Ashtiani and J. A. Papin, Mol Syst Biol, 2011, 7, 518.

2. H. Yu, Y. Xia, V. Trifonov and M. Gerstein, Genome Biol, 2006, 7, R55.3. S. F. Altschul, W. Gish, W. Miller, E. W. Myers and D. J. Lipman, Journal of molecular

biology, 1990, 215, 403-410.4. S. Balaji, M. M. Babu and L. Aravind, Journal of molecular biology, 2007, 372, 1108-1122.5. M. B. Eisen, P. T. Spellman, P. O. Brown and D. Botstein, Proceedings of the National

Academy of Sciences of the United States of America, 1998, 95, 14863-14868.6. S. Mintz-Oron, S. Meir, S. Malitsky, E. Ruppin, A. Aharoni and T. Shlomi, Proceedings of the

National Academy of Sciences, 2012, 109, 339-344.7. A. M. Altenhoff, A. Schneider, G. H. Gonnet and C. Dessimoz, Nucleic Acids Research, 2011,

39, D289-D294.8. S. Maere, K. Heymans and M. Kuiper, Bioinformatics, 2005, 21, 3448-3449.9. Y. Bilu, T. Shlomi, N. Barkai and E. Ruppin, PLoS Comput Biol, 2006, 2, e106.10. F. Merchán, H. van den Ende, E. Fernández and C. F. Beck, Planta, 2001, 213, 309-317.11. K. Motojima, S. Kanaya and S. Goto, Journal of Biological Chemistry, 1988, 263, 16677-

16681.12. I. Kimiyoshi, A. Yoshihiro, N. Kumi, M. Shinsei, H. Tatsuo, S. Osamu, S. Nobuyoshi and N.

Takeshi, Gene, 1993, 133, 279-284.

25