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2 Microbiology of Composting HANS JÜRGEN KUTZNER Ober-Ramstadt, Germany 1 Introduction 36 2 Heat Production by Microorganisms 37 3 The Phases of the Composting Process 40 4 The Compost Pile as a Microbial Habitat 42 4.1 Organic Wastes as Nutrients 43 4.2 Water Availability 45 4.3 Structure, Oxygen Supply and Aeration 46 4.4 Temperature 47 4.5 Hydrogen Ion Concentration, pH 48 5 Laboratory Composting 49 6 The Microorganisms of Composting 54 6.1 The Main Groups of Microbes Active in Composting 56 6.1.1 Bacteria 59 6.1.2 Actinomycetes 60 6.1.3 Fungi 64 6.2 Microbial Successions in Composting 65 7 Hygienic Aspects of Composting 70 7.1 Inactivation of Pathogens 70 7.2 Emission of Microorganisms from Composting Plants 72 8 Phytopathogenic Aspects of Composting 76 8.1 Inactivation of Plant Pathogens during Composting 77 8.2 Adverse Effects of Fresh, Immature Compost on Plant Growth 77 8.3 Control of Soilborne Plant Pathogens by Compost 77 8.4 Control of Foliar Diseases by Compost Water Extracts 78 9 Balancing the Composting Process 78 9.1 Mass Balance 79 9.2 Energy Balance and Heat Transfer 82 9.3 Heat Recovery from Composting Plants 85 9.4 Mathematical Modeling of the Composting Process 87 10 Odor Formation and Control 87 11 Compost Maturity 89 12 References 90

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Page 1: v11c_comp_trial

2 Microbiology of Composting

HANS JÜRGEN KUTZNEROber-Ramstadt, Germany

1 Introduction 362 Heat Production by Microorganisms 373 The Phases of the Composting Process 404 The Compost Pile as a Microbial Habitat 42

4.1 Organic Wastes as Nutrients 434.2 Water Availability 454.3 Structure, Oxygen Supply and Aeration 464.4 Temperature 474.5 Hydrogen Ion Concentration, pH 48

5 Laboratory Composting 496 The Microorganisms of Composting 54

6.1 The Main Groups of Microbes Active in Composting 566.1.1 Bacteria 596.1.2 Actinomycetes 606.1.3 Fungi 64

6.2 Microbial Successions in Composting 657 Hygienic Aspects of Composting 70

7.1 Inactivation of Pathogens 707.2 Emission of Microorganisms from Composting Plants 72

8 Phytopathogenic Aspects of Composting 768.1 Inactivation of Plant Pathogens during Composting 778.2 Adverse Effects of Fresh, Immature Compost on Plant Growth 778.3 Control of Soilborne Plant Pathogens by Compost 778.4 Control of Foliar Diseases by Compost Water Extracts 78

9 Balancing the Composting Process 789.1 Mass Balance 799.2 Energy Balance and Heat Transfer 829.3 Heat Recovery from Composting Plants 859.4 Mathematical Modeling of the Composting Process 87

10 Odor Formation and Control 8711 Compost Maturity 8912 References 90

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36 2 Microbiology of Composting

List of AbbreviationsAPPL acid precipitable, polymeric ligninCFU colony forming unitGC gas–liquid chromatographyHDMF 3-hydroxy-4,5-dimethyl-2(5H)-furanoneMS mass spectroscopyPVC polyvinyl chlorideSAR systemic acquired resistanceTMV tobacco mosaic virusTOC total organic compoundv.s. volatile solids

1 IntroductionIn his comprehensive monographs, HAUG

(1980, 1993) defines composting as “the bio-logical decomposition and stabilization of or-ganic substrates under conditions which allowdevelopment of thermophilic temperatures as aresult of biologically produced heat, with a finalproduct sufficiently stable for storage and ap-plication to land without adverse environmen-tal effects”. This definition differentiates com-posting from the mineralization of dead or-ganic matter taking place in nature above thesoil or in its upper layers leading to a more orless complete decomposition – besides the for-mation of humic substances; it thus describesthe compost pile as a man-made microbialecosystem. Composting has been carried outfor centuries, originally as an agricultural andhorticultural practice to recycle plant nutrientsand to increase soil fertility (HOWARD, 1948);nowadays it has become also part of the man-

agement of waste disposal to get rid of thehuge amounts of diverse organic waste pro-duced by our civilized urban life. In most cases,the product compost has to be regarded as aby-product which hardly finances its produc-tion now often being carried out in highlymechanized plants (FINSTEIN et al., 1986; FIN-STEIN, 1992; JACKSON et al., 1992; STEGMANN,1996).

Composting has frequently been regardedas more an art than a science; this view, howev-er, ignores the fact that its scientific base iswell understood; of course, successful applica-tion of the principles requires experience as ismore or less true for all applied sciences. Infact, the basic rules of composting have beenknown for decades as can be seen from nu-merous reviews and monographs of the last 25years, beginning with UPDEGRAFF (1972) andending with DE BERTOLDI et al. (1996). Thesesurveys also indicate the broad interest of sci-entists of various disciplines in this process,

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2 Heat Production by Microorganisms 37

disciplines such as agriculture, horticulture,mushroom science, soil science, microbiologyand sanitary engineering. The literature oncomposting is vast, comprising numerous broadreviews and minireviews of which only few canbe cited in addition to those mentioned above:GASSER (1985), BIDDLESTONE et al. (1987), MA-THUR (1991), MILLER (1991, 1993), HOITINK andKEENER (1993) and SMITH (1993); in addition,there exist also specific journals devoted solelyor primarily to the subject, e.g., “Compost Sci-ence”, “Agricultural Wastes”, “Müll & Abfall”.Being well aware of the literature covered inthese reviews, the author has tried to avoid rep-etition as much as possible; thus only selectedpapers will be considered, in addition to payingregard to some older work not reviewed untilnow because of its “hidden” publication.

This review is primarily concerned with themicrobiology of composting. However, sincecomposting touches many related disciplines,even the restriction to this selected field has totake various aspects into consideration whichmay seem at first glance rather remote fromthe composting process per se:

(1) The microbiology of self-heating ofmoist, damp organic matter has firstbeen extensively studied in the case ofagricultural products, e.g., hay, grain andwool. This phenomenon very early ledto the concept of heat generation aspart of microbial (and organismic ingeneral) metabolism.

(2) The microbiology of composting issomehow related to soil microbiologyand litter decomposition, i.e., soil fertil-ity, turnover of organic matter in natureand formation of humic substances.

(3) The control of pathogenic agents inwastes to be composted, and the emis-sion of pathogenic agents from compostplants are of concern to medical micro-biologists. This aspect has to be extend-ed to agents causing plant diseases andto the effect of compost on plant patho-gens.

(4) Mushroom cultivation includes thepreparation of a compost substrate, aspecial process whose study contributedmuch to the general understanding ofcomposting.

The main focus of this chapter will be the com-post pile as a microbial ecosystem, and a moreproper title for it would be “A Microbiologist’sView of Composting”. Most of the reviews cit-ed above also deal with the microbiology ofcomposting, and there are several which spe-cifically discuss this aspect, e.g., FINSTEIN andMORRIS (1975) and LACEY (1980). Many pa-pers mentioned there will not be cited in thisreview, and it is hoped that their authors willhave some understanding for this approach: areviewer has to make a selection of topics andof the literature to be cited, which inevitablyleads to a somewhat personal view, not entire-ly free of bias.

2 Heat Production byMicroorganisms

Any metabolism – from microbes to man –leads inevitably to the production of heat (Fig.1, Tab. 1). This is actually a consequence of the2nd law of thermodynamics, i.e., only part ofthe energy consumed can be transformed intouseful work, e.g., biosynthesis, while the rest isliberated as heat to increase the entropy of thesurroundings. Very often, mostly just for sim-plification, the degradation of a carbohydrate(e.g., glucose) serves as an example to demon-strate this context: Tab. 2 gives an energy bal-ance for the aerobic metabolism of 2 M glu-cose, assuming that 1 of them enters the ener-gy metabolism producing 38 ATP M–1 glucose,whereas the other supplies the precursors forthe biosynthesis of new biomass which con-sumes the 38 ATP: According to this calcula-tion, which follows the reasoning of DIEKERT

(1997), the catabolism has a physiological effi-ciency of 61–69%, whereas the anabolism ofonly 40%. A very similar balance has beenfound by TERROINE and WURMSER (1922) forthe mold Aspergillus niger as discussed in de-tail by BATTLEY (1987, pp. 108 ff): 59% of theenergy (not weight!) of the glucose consumedwere incorporated into new biomass (myceli-um), whereas 41% were liberated as heat.

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38 2 Microbiology of Composting

Energy content ofall nutrients utilized

% (?)Flow to anabolism

% (?)Flow to catabolism

40% as heat

60% in ATP

60% as heat

CO2 + H2O

40%

O2

Energy contentof produced

biomass(a) for formation of monomers(b) for formation of polymers(c) for other cell activities

Fig. 1. Energy flowin aerobic metab-olism of bacteria(for further explana-tion see text andTab. 1).

Tab. 1. Energy flow in Microorganisms with Glucose as Substrate: Proportioning of the Substrate Energy toNew Biomass and Liberated Heat as well as especially the YATP Value Depend on the Number of ATP perMol Glucose

% Glucose Utilized for % Substrate Energy in

Catabolism Anabolism New Liberated ATP Ys YATP

(Energy (Biosyn- Biomass Heat Glucose–1

Production) thesis)

A 25 75 81.1 18.9 38 0.565 10.7B1 33.33 66.66 74.8 25.2 38 0.502 7.137B2 33.33 66.66 72.2 27.8 26 0.502 10.43C1 50 50 62.2 37.8 38 0.376 3.568C2 50 50 58.3 41.7 26 0.376 5.215

Tab. 2. Energy Balance of the Aerobic Metabolism of Glucose by Bacteria (Free Energy of HydrolysisATPcH2O ] ADPcPi: Ap52 kJ, Bp46 kJ)

Metabolism A B

Catabolic metabolismC6H12O6c6 O2 ] 6 CO2c6 H2O D G01pP2,872 kJInvested into 38 ATP (38 · 52 or 46 kJ) D G01pP1,976 kJp69% 1,748 kJp61%Liberated as heat D G01pP1,896 kJp31% 1,124 kJp39%

Anabolic metabolismFree energy of hydrolysis of 38 ATP D G01pP1,976 kJInvested in biosynthesis, transport, movement D G01pP1,790 kJp40% 1,699 kJp40%Liberated as heat D G01pP1,186 kJp60% 1,049 kJp60%

Total balance2 M glucose (2 · 2,872) D G01pP5,744 kJLiberated as heat D G01pP2,082 kJp36% 2,173 kJp38%Fixed in new biomass D G01pP3,662 kJp64% 3,571 kJp62%

Note that the heat of combustion of 1 M glucose amounts to D HcpP2,816 kJ.

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2 Heat Production by Microorganisms 39

The percentages of the substrate (1) em-ployed for energy formation (catabolism) and(2) utilized for biosynthesis depend on the en-ergy source and the kind of metabolism, (e.g.,amount of ATP M–1 substrate).

For E. coli (26 ATP M–1 glucose) DIEKERT

(1997) proposed the following balance: Onethird of the substrate (glucose) is used for theproduction of ATP, whereas two thirds [morecorrectly 4 of the 6 carbon atoms (Eq. 1)] ap-pear in the biomass; this results in an Ys ofabout 0.5 and an YATP of about 10 (Tab. 3).

The heat produced in the metabolism of mi-crobes cultivated on a small scale is rapidly dis-sipated to the environment and hardly noticedin laboratory experiments. Therefore, this phe-nomenon, although of great theoretical impor-tance, is surprisingly not discussed in mosttextbooks of microbiology, a rare exceptionbeing the one by LAMANNA and MALLETTE

(1959, pp. 586–589). Of course, heat productionis of great practical significance in the massculture of microorganisms and, therefore,treated in books on biochemical engineering,e.g., BAILY and OLLIS (1977, pp. 473–482) andCRUEGER and CRUEGER (1984, pp. 58–59); ithas been extensively discussed by LUONG and

Tab. 3. Equations of Microbial Growth Calculated for Various Growth Efficiencies

(1) C6H12O6c0.8 NH3c2.0 O2 ] 0.8 [C5H7O2N]c2.0 CO2c4.4 H2O Ysp90.4/180p0.502(2) C6H12O6c0.7 NH3c2.5 O2 ] 0.7 [C5H7O2N]c2.5 CO2c4.6 H2O Ysp79.1/180p0.430(3) C6H12O6c0.6 NH3c3.0 O2 ] 0.6 [C5H7O2N]c3.0 CO2c4.8 H2O Ysp67.8/180p0.376(4) C6H12O6c0.5 NH3c3.5 O2 ] 0.5 [C5H7O2N]c3.5 CO2c5.0 H2O Ysp56.5/180p0.314(5) C6H12O6c0.4 NH3c4.0 O2 ] 0.4 [C5H7O2N]c4.0 CO2c5.2 H2O Ysp45.2/180p0.251(6) C6H12O6c0.3 NH3c4.5 O2 ] 0.3 [C5H7O2N]c4.5 CO2c5.4 H2O Ysp33.9/180p0.188(7) C6H12O6c0.2 NH3c5.0 O2 ] 0.2 [C5H7O2N]c5.0 CO2c5.6 H2O Ysp22.6/180p0.125

HAUG (1993, p. 248) considered Ysp0.1–0.2 as a typical growth yield in composting; for Ysp0.1 he presented the following balance (here reduced to one mole of glucose).

(8) C6H12O6c0.16 NH3c5.2 O2 ] 0.16 [C5H7O2N]c5.2 CO2c5.7 H2O Ysp18.8/180p0.104

1. Note: Calculation in g (NB p New Biomass)

(a) Complete oxidation of glucose without production of biomass100 g glucosec106,7 g O2 ] 146.7 g CO2c60 g H2O

(b) Eqs. (1) and (6) from above in g:Ysp0.502 : [100c7.5] substratec35.6 O2 ] 50.2 NBc48.9 CO2c44.0 H2OYsp0.188 : [100c2.8] substratec80.0 O2 ] 18.8 NBc110.0 CO2c54.0 H2O

(c) The following equation has been used for the hypothetical composting process discussed inSect. 9 (Fig. 15 and Tab. 15, Equ. 8aYsp0.2008 : [100c3.02] substratec78.22 ] 20.08 NBc107.56 CO2c53.6 H2O

2. Note Calculation of oxygen consumption in relation to loss of volatile solids, D v.s., in g:Ysp0.502 : D v.s.p107.5P50.2p57.3c35.6 O2 ] 48.9 CO2c44.0 H2O

D v.s. : 100c62.13 O2 ]85.34 CO2c76.79 H2OYsp0.188 : D v.s.p102.8P18.8p84.0c80.0 O2 ] 110.0 CO2c54.0 H2O

D v.s. : 100c95.23 O2 ]130.95 CO2c64.28 H2OYsp0.167 : D v.s.p102.5P16.7p85.8c83.0 O2 ] 114.1 CO2c54.7 H2O

D v.s. : 100c96.73 O2 ]132.98 CO2c63.75 H2O

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VOLESKY (1983), in the monograph by BATT-LEY (1987) and in Vol. 1 of the Second Editionof Biotechnology by POSTEN and COONEY

(1993, pp. 141–143).

3 The Phases of theComposting Process

If the heat produced by the metabolism ofmicroorganisms is prevented by some kind ofinsulation from being dissipated to the envi-ronment, the temperature of the habitat in-creases. This is the case when damp organicmatter is collected in bulky heaps or kept intight containers, as it is done when organicwaste is composted either in large piles (win-drows) or in boxes of various kinds. If the com-posting process is carried out as a batch culture– as opposed to a continuous operation – itproceeds in various more or less distinct phas-es which are recognized superficially by thestages of temperature rise and decline (Fig. 2).These temperature phases are, of course, onlythe reflection of the activities of successive mi-crobial populations performing the degrada-tion of increasingly more recalcitrant organicmatter.

As shown in Fig. 2, the time–temperaturecourse of the composting process can be divid-ed into 4 phases:

(1) During the first phase a diverse popula-tion of mesophilic bacteria and fungiproliferates, degrading primarily thereadily available nutrients and therebyraising the temperature to about 45 °C.At this point their activities cease, thevegetative cells and hyphae die andeventually lyse, and only heat resistantspores survive.

(2) After a short lag period (not always dis-cernible) there occurs a second more orless steep rise of temperature. This sec-ond phase is characterized by the devel-opment of a thermophilic microbialpopulation comprising some bacterialspecies, actinomycetes and fungi. Thetemperature optimum of these microor-

ganisms is between 50 and 65 °C, theiractivities terminate at 70–80 °C.

(3) The third phase can be regarded as astationary period without significantchanges of temperature because micro-bial heat production and heat dissipa-tion balance each other. The microbialpopulation continues to consist of ther-mophilic bacteria, actinomycetes, andfungi.

(4) The fourth phase is characterized by agradual temperature decline; it is bestdescribed as the maturation phase ofthe composting process. Mesophilic mi-croorganisms having survived the hightemperature phase or invading thecooling down material from the outsidesucceed the thermophilic ones and ex-tend the degradation process as far as itis intended.

Fig. 2 presents just one of numerous examplesof the temperature course that can be found inthe literature, very typical ones having beenpublished by CARLYLE and NORMAN (1941),WALKER and HARRISON (1960), NIESE (1959).In all cases the 4 phases mentioned have beenobserved more or less distinctly leaving nodoubt that they characterize very closely thecomposting process.

Since the optimum temperature for com-posting is regarded to be about 50–60 °C,measures are being taken to prevent furtherself-heating except for a rather short period upto 70 °C to guarantee the elimination of patho-gens (see Sect. 7.1). However, 70 °C appears tobe not the limit of microbial heat productionwhich can easily reach 80 °C as practised in theBeltsville process (see Sect. 4.3). Under certainconditions even much higher temperaturesleading to ignition can be reached, but neitherthe exact requirements for such an event northe mechanism of ignition appear to be wellunderstood (BOWES, 1984). Whereas there areonly rare cases of self-ignition of manure pilesor compost heaps (JAMES et al., 1928), this phe-nomenon is not uncommon in the storage ofdamp hay (GLATHE, 1959, 1960; CURRIE andFESTENSTEIN, 1971; HUSSAIN, 1972) and fatcontaminated pie wool (WALKER and WIL-LIAMSON, 1957).

40 2 Microbiology of Composting

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3 The Phases of the Composting Process 41

As mentioned above the temperature phas-es are just a reflection of the activities of suc-cessive microbial populations. This has beendemonstrated by various means – besides by adetailed analysis of the bacterial, actinomyceteand fungal population:

(1) Fig. 3, taken from NIESE (1969), showsthat the microbial community of freshrefuse plus sewage sludge exhibits arespiratory activity only at 28 and38 °C, i.e., it consists primarily of meso-philes. On the contrary, the samples tak-en from the self-heated material startedinstantaneously to take up oxygenwhen incubated at 58 and 48 °C; the rel-atively high respiration rate at 38 °C isprobably due to the broad temperaturerange of several thermophiles (Sect. 6,Fig. 8, Tab. 9).

(2) Fig. 4, taken from FERTIG (1981), illus-trates the O2 uptake and CO2 produc-

tion during the temperature course ofcomposting: 4 maxima of microbial ac-tivity can be observed, surprisinglywithin the very short time of 54 h. Twoor three maxima of CO2 evolution dur-ing composting have been observed bynumerous authors, e.g., SIKORA et al.(1983) who discussed also earlier obser-vations of this kind; VIEL et al. (1987)reported three maxima of oxygen con-sumption.

(3) Finally, a detailed analysis of adaptationand succession of microbial populationsin composting of sewage sludge hasbeen undertaken by MCKINLEY andVESTAL (1984, 1985a,b), the main aimof their study being to ascertain the op-timal temperature for the compostingprocess: The microbial communitiesfrom hotter samples were better adapt-ed to higher temperatures than thosefrom cooler samples and vice versa, as

Fig. 2. Temperature course during the composting of urban garbage: four phases, mesophilic, thermophilic,stationary, and maturation, can easily be recognized (from PÖPEL, 1971).

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shown by the determination of the rateof [14C]-acetate incorporation into cel-lular lipids and calculation of its appar-ent energies of activation and inactiva-tion. Lipid phosphate was used as indi-cator of viable bacterial biomass. Theauthors came to the conclusion, that thecomposting temperature should not beallowed to exceed 55 °C – in agreementwith numerous other investigators.

42 2 Microbiology of Composting

Fig. 3a,b. Oxygen uptake of microbial communitiesin Warburg flasks at different temperatures: A freshgarbage plus sewage sludge, B composting materialremoved from the pile during the high temperaturephase, 28 °C 38 °C 48 °C 58 °C (according to NIESE, 1969).

4 The Compost Pile as aMicrobial Habitat

In order to secure fast stabilization of thewaste material, the microorganisms perform-ing this task have to be provided with nutrients,water and oxygen. Of course, the demand fornutrients appears to be contradictory sincematerial without nutrients does not need to bestabilized. However, because organic wastematerial in any case lends itself to decomposi-tion the nutritional state of the starting materi-al deserves consideration.

A fourth parameter of composting is thetemperature, which plays actually a dual role inthis habitat: It is the result of microbial activity– without necessity of being taken care of atthe commencement of the process – and at thesame time it is a selective agent determiningthe microbial population at any stage of thecomposting process, eventually demanding itsregulation by technical measures.

Finally, the pH of the habitat can be consid-ered as environmental factor.

It is obvious that the various parameters areintimately related; this should be kept in mindwhen in Sects. 4.1–4.5 they are necessarilytreated separately.

4.1 Organic Wastes as Nutrients

Waste suitable for composting comes fromvery diverse sources: grass clippings, leaves,hedge cuttings, food remains, fruit and vegeta-bles waste from the food industry, residuesfrom the fermentation industry, solid and liq-uid manure from animal houses, wastes fromthe forest, wood and paper industries, rumencontents from slaughtered cattle and sewagesludge from wastewater treatment plants.Thus, the starting material of composting var-ies tremendously in its coarse composition,and in addition there is often a seasonal varia-tion of the material arriving at the compostplant. Since many of the materials listed abovecannot be easily composted if supplied bythemselves alone because of nutritional and/orstructural reasons (water content), they have

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4 The Compost Pile as a Microbial Habitat 43

to be mixed purposely if they are not deliveredas a mixture in the first place.

Tables listing the chemical composition ofthe materials mentioned, e.g., contents of car-bohydrates, proteins, fat, hydrocarbons, ligninand ash are given by BIDLINGMAIER (1983),and KROGMANN (1994), and can be found invarious reviews cited above. Unfortunately,the data of most of the ingredients are ratherincomplete making a strict comparison diffi-cult. These tables sometimes contain empiricalformulae of the substrates involved, e.g., forsewage sludge [C10H19O3], for the organicfraction of domestic garbage [C64H104O37N]for residues from vegetables [C16H27O8N], andfor grass [C23H38O17N]. However, these fig-ures are almost meaningless, except that theyindicate the carbon–nitrogen ratio (see alsoSect. 9.1, Tab. 16).

Of greater relevance is the biochemicalcomposition of the various waste materials be-cause this determines their susceptibility tomicrobial degradation. Those wastes contain-ing carbohydrates, lipids and proteins, wouldbe the most suitable carbon and energy sourc-es for microbes, whereas materials with a high

lignocellulose fraction and a shortage of ni-trogenous compounds will be only slowly de-graded. In fact, the biodegradability of organicmatter in composting may be related to the lig-nin content (HAUG, 1993, pp. 312–314) em-ploying a formula which has been derivedoriginally for anaerobic digestion by CHAND-LER et al. (1980):

biogradable fraction of volatile solids (v.s.)p0.830–0.028 x lignin content in % of v.s. (9)

According to this formula a substrate contain-ing no lignin would only achieve a maximumdegradability of 83% because the decomposi-tion of the substrate organics is coupled withproduction of bacterial by-products, some ofwhich themselves are not readily degradable.However, since the waste material has to sup-port the growth of several successive microbialpopulations, which have different nutritionalrequirements and different capabilities to at-tack macromolecules of organismic origin, thewaste material need not (and, in fact, shouldnot) consist solely of easily degradable materi-als.

Fig. 4. Oxygen uptake and CO2 production during laboratory composting:four maxima occurring within the first 2 d (!) are easily recognized (accord-ing to FERTIG, 1981).

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It can be more or less safely assumed thatthe starting materials – at least mixtures ofthose listed above – contain the essential nutri-ents or elements for microbial growth. Where-as carbon compounds for energy metabolismand biosynthesis are in most cases in excess,the nitrogen supply is usually rather limited. Infact, the carbon–nitrogen ratio is considered asignificant criterion of the starting material aswell as of the product compost. A rule ofthumb says that the C–N ratio at the beginningof composting should be about 30 :1 and willbe reduced to about 10 :1 in the course of theprocess. Of course, there is a theory behind thisempirical recommendation which has beenseldom considered: The decrease of the C–Nratio can only be understood if we assume thatthere are several microbial populations, eachdeteriorating at the end of its growth phaseand supplying its nitrogen to the next popula-tion.The factor by which this process advancesdepends on three parameters:

(1) the C–N ratio of the new biomass,(2) the yield coefficient Ys, and(3) the rate of turnover of the biomass; the

latter is, however, a matter of conjec-ture.

In Fig. 5, Tab. 4 a bacterial biomass of[C5H7O2N] is assumed (C–N ratio 4.28), and aC turnover rate of 75%; the calculation hasbeen carried out for seven yield coefficients,using the conception depicted in Tab. 5.

As mentioned above, the rate of biomassturnover is open for discussion. However,

whichever reasonable value will be employed,the result will correspond to Fig. 5, Tab. 3, onlythe slope of the straight lines varying. Fromthis figure it can be deduced that at Ysp0.5four succeeding populations reduce the C–Nratio from 25.7–12.8; at the same time, they de-compose 50% of the organic matter. The samecalculation can be done with fungal biomass[C10H18O5N], C–N ratiop8.57: In this case,

44 2 Microbiology of Composting

Fig. 5. The stepwise decrease of the C–N ratio bysucceeding populations of bacteria (carbon turnoverrate of the cell biomass=75%), values see Tab. 4.

Tab. 4. Stepwise Decrease of the C–N Ratio by Succeeding Populations of Bacteria (Fig. 5)

Ys Decrease per Population Narrowing the ConcomitantD Volatile D C–N Ratio by Degradation ofSolids C–N A–F: 4 Populations Volatile Solids(as Glucose) G: 3 Populations in % (as Glucose)

A 0.565 78.75 2.50 23.5 ] 13.6 43B 0.502 90.00 3.21 25.7 ] 12.8 50C 0.439 101.25 4.13 28.5 ] 11.9 58D 0.376 112.50 5.36 32.1 ] 10.7 67E 0.313 123.75 7.07 37.3 ] 9.0 76F 0.251 135.00 9.64 45.0 ] 6.4 86G 0.188 146.25 13.93 57.8 ] 16.1 72

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4 The Compost Pile as a Microbial Habitat 45

three populations (Ysp0.52) diminish theC–N ratio from 32.1–12.8, degrading concomi-tantly 60% of the volatile solids.

Since the carbon–nitrogen ratio of the vari-ous types of the waste material deviates fromthe ratio considered optimum, they have to bemixed to arrive at a value which is required tolead – at least theoretically – to the fixation ofthe nitrogen in new biomass and in humic sub-stances, or as ammonium adsorbed by inorgan-ic and organic particles. Otherwise, nitrogen inexcess will be lost as NH3 to the air. If, on theother hand, nitrogen is deficient, the compostwhen applied as fertilizer will lead to the so-called nitrogen depression well known tofarmers, i.e., soil nitrogen instead of beingavailable for plant growth will be used for thefurther degradation of surplus carbon andthereby temporarily incorporated into micro-bial biomass.

4.2 Water Availability

General experience shows that organic mat-ter can be stored without any risk of deteriora-tion if kept dry, e.g., containing less than about12% of moisture. In fact, drying is the most an-cient method to preserve foodstuffs and ani-mal feed. Less thorough drying (or inadvertentwetting) leads to instantaneous growth of mi-croorganisms inherent in any organic matter(if not intentionally sterilized). Thus, water iscertainly the initiator of microbial develop-ment on dead organic matter.

The water–microbe relationships in a com-post pile are manifold. One would expect thatthere is an optimum moisture content on amere weight basis, but this is not the case. Thisis because water exists in different states which

are unequally available to microbes: waterfilms covering the solid particles, capillary wa-ter, and matrix water. The various materials tobe composted differ widely in their waterholding capacity; i.e., the same moisture con-tent in % of dry matter can result in a very dif-ferent water availability. Thus, some materialsrequire for optimum composting a water con-tent of 75–90% (saw dust, straw), whereas oth-ers (grass clippings, food remains) need only awater content of 50–60%.Therefore, two othercriteria are more suitable to characterize thewater status:

(1) the water activity, expressed by the so-called aw value (aw: vapor pressure ofwater in a solution/vapor pressure ofpure water.

(2) the water potential C (more exactly“potential energy of water”) which isrelated to the aw value by Eq. (10)(TEMPLE, 1981):

CpRT Vw–1 · ln aw

(dimension kg m–2) (10)

Vw: partial molal volume of water.

Water activity is always less than 1.0, and waterpotential is always negative in real systems,since they express the availability of water inthe real system contrasted to the availability ofpure water under the same conditions.

The use of water activity to characterize thewater status of a system has now been widelyreplaced by the measurements of the water po-tential, as outlined by PAPENDICK and MULLA

(1986). This is, because water activity is muchtoo insensitive in systems with a high amountof readily available water; instead, the water

Tab. 5. Calculation of the Decrease of the C–N Ratio of the Nutrient Supply by the Growth of One Bacte-rial Population at a 75% Carbon Turnover Rate and Ysp0.502 (see Eq. 1 in Tab. 3)

Start (C6H12O6)4c0.8 NH3 C–Np288 (11.2)–1p25.71Growth (C6H12O6)1c0.8 NH3c2 O2 ] 0.8 [C5H7O2N]c2 CO2c4.4 H2OLysis/turnover 0.8 [C5H7O2N]c1 O2c1.4 H2O ] 0.5 glucosec0.8 NH3c1 CO2

Balance (C6H12O6)4c0.8 NH3c3 O2 ] (C6H12O6)3.5c0.8 NH3c3 CO2c3 H2ORest for next population (C6H12O6)3.5c0.8 NH3 C–Np252 (11.2)–1p22.5

D M glucosep4P3.5p0.5p90 g “volatile solids”; D C–Np3.21.

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potential is regarded as the only approach forinvestigating water limitations caused by dry-ness, as discussed in detail by MILLER (1989,1991) and DIX and WEBSTER (1995, pp.59–66). Water potential is made up of severalcomponents, i.e., osmotic, matric, pressure andgravimetric. In composting systems, the matrixwater potential (as measured with a tensiome-ter and expressed as a negative pressure inunits of pascals [Pa]) is the most importantone; it determines the extent of filling of thecapillaries with water: a potential of P20to P50 kPa is regarded as optimal, whereasP5 kPa stand for a too wet matrix, andP100 kPa for a too dry matrix. At P300 kPapores of just ^1 µm are water saturated, andP1,380 kPa correspond to the wilting point ofvascular plants; this latter value is equivalentto a water activity of 0.990.

Apart from being essential for microbialgrowth, the moisture content of the startingmaterial influences the course of the compost-ing process: Too high a content hinders aera-tion and thus reduces the supply of oxygen foraerobic microbial growth, thereby favoring theestablishment of anaerobic niches with theconsequence of anaerobic metabolism leadingto the formation of acid fermentation prod-ucts. Even more important, however, is the factthat a high water content delays the self-heat-ing because of the relatively high heat capacityof water. On the other hand, too little water,which of course can be easily corrected, re-tards the composting process.

The water content of the starting material isonly one aspect of water and composting. Infact, the dynamics of water changes within acompost pile are rather complex. First, water isproduced by aerobic microbial metabolism,about 0.45 kg of water per 1.0 kg of decom-posed organic material. MILLER (1991) collect-ed five values from the literature which aresomewhat higher: WILEY and PEARCE (1957):0.63 g H2O g–1 garbage decomposed; GRIFFIN

(1977): 0.55 g H2O g–1 cellulose, HAUG (1979):0.72 g H2O g–1 sewage sludge; HOGAN et al.(1989): 0.5–0.53 g H2O g–1 rice hullscriceflour; HARPER et al. (1992) 0.5–0.6 g H2O g–1

straw and poultry manure. (Although this isnot of great influence in composting, this effecthas to be considered when storing foods andfeeds just at the threshold of the moisture re-

quirements of microbial growth.) – Second,water is continually removed from the com-post by the air supplied to meet the oxygen de-mand of the microorganisms and to removeheat from the compost pile to avoid tempera-tures above 60–70 °C. This withdrawal of wa-ter, which is actually desirable, must, of course,not proceed faster than the composting pro-cess, i.e., before the material is “stabilized”;otherwise, water has to be added for optimumcompletion of the process. At any rate, the wa-ter content of the compost pile decreases dur-ing the process, let’s say from 50–70% to about30%.This leads to a reduction of the microbialacitivities in general, but to an encouragementof microbes adapted to rather dry conditions,e.g., xerophilic fungi (DIX and WEBSTER, 1995,pp. 332–340).

4.3 Structure, Oxygen Supply andAeration

The aerobic decomposition of organic mat-ter requires oxygen in a definite stoichiometricrelation. According to an equation, which willbe used in Sect. 9.1, Tab. 15 for balancing theprocess, about 80 g of oxygen are used up forthe degradation of 100 g of organic matter. Itcan be easily imagined that this amount is notinitially contained in the compost pile and thatit hardly reaches its interior just by passive dif-fusion.Thus, a very active aeration is necessaryfor an effective composting process. However,aeration has to fulfill another purpose which,as it turns out, is quantitatively of even greaterimportance: In a well isolated compost pile, thetemperature can soon reach 80 °C and evenhigher. This is not compatible with microbiallife, thus leading to microbial suicide (FIN-STEIN, 1989). This heat has to be removedby ventilative cooling. As will be shown inSect. 9.2 about 5 times as much air are neededfor the removal of the heat as for the supply ofthe oxygen necessary for microbial metab-olism.

Before further discussing aeration, anotheraspect has to be dealt with, i.e., the structure ofthe compost pile. This topic has been studiedextensively by SCHUCHARDT (1977): The com-post pile is a 3-phasic system comprising solid

46 2 Microbiology of Composting

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4 The Compost Pile as a Microbial Habitat 47

matter, water and gas. For optimum perfor-mance of the process, the free air space shouldamount to 20–30% of the total volume. Since,in the course of composting, this value tends todecrease, it has to be kept that way by a repeat-ed turning over of the pile. By this means alsolarger air channels, which are often built-up,are destroyed. The relationship between porevolume (water and gas volume) and volume ofsolid matter does not describe the system com-pletely because the variance of particle size, ofdiameters of air channels, and of capillariespenetrating the individual particles finally de-termine the provision of the microbial popula-tion with oxygen. Oxygen reaches the microbi-al cells by a succession of various mechanisms:convection and diffusion within the free airspace, and dissolution in the liquid phase. Evenif thoroughly aerated, it appears that anaero-bic microniches are left, allowing anaerobicmicrobial metabolism; thus, in practice com-posting appears to be not an entirely aerobicprocess (DERIKX et al., 1989; ATKINSON et al.,1996).This can be deduced from the formationof organic acids, leading to a drop of pH (espe-cially during the first phase), and the appear-ance of traces of gases from anaerobic metab-olism in the exhaust air, e.g., methane and N2O(denitrification) (HELLMANN et al., 1997; LEI-NEMANN, 1998).

The amount of air to be supplied to a com-post pile, usually measured in m3 air kg–1 dryorganic matter h–1, is certainly a matter ofpractical experience. Of course, the uptake ofoxygen by microbial metabolism can now beanalyzed on-line, giving information about thedegradative activity; alternatively, and possiblymore conveniently, the CO2 content of the ex-haust air can be determined. According toStrom et al. (1980) the O2 content of the ex-haust air should not drop below 5%, andBIDLINGMAIER (1983) regards 10% as toler-able. DE BERTOLDI et al. (1983) recommendeven 18% O2, whereas SUHLER and FINSTEIN

(1977) found no difference in composting effi-ciency between 10 and 18% O2 in the exhaustair.

Aeration based on oxygen consumption hasbeen one of the possible strategies for control-ling the composting process, i.e., the Beltsvilleprocess. This approach, however, has beenstrongly opposed by FINSTEIN et al. (1986),

who convincingly showed that aeration isquantitatively more important for regulatingthe temperature of the compost pile by ventila-tive cooling (Rutgers strategy) than for supply-ing oxygen to the microbes (see also Sect. 9.2).Since much more air is necessary to meet thisrequirement, any considerations regarding theamount of oxygen needed for the decomposi-tion of organic matter are secondary. In addi-tion, only part of the organic matter is degrad-ed during a certain stage (and this is notknown in advance, unless O2–CO2 analysis ofthe exhaust air is carried out on-line). There-fore, the oxygen requirement to be met cannotbe calculated exactly to arrive at an optimumaeration. The wide variation of organic wastein its composition and, thus, in its degradabilityadds further uncertainty. And finally, since theefficiency of the air supply to carry out its tasksdepends also on the structure of the waste ma-terial, the wide range of values for “optimum”composting to be found in the literature is notsurprising. Of course, the engineer planning acomposting plant must have some guidance tocalculate the aeration devices, but these calcu-lations can hardly be based on pure microbio-logical or thermodynamical data.

4.4 Temperature

Since production of heat and its preserva-tion within the compost pile – at least for a cer-tain period of time – is an outstanding charac-teristic of the composting ecosystem as com-pared with other terrestrial habitats, the pa-rameter temperature has found the specialinterest of compost microbiologists and com-posting practitioners. The temperature rela-tionship of microorganisms are dealt with innumerous treatises (e.g., INGRAHAM, 1962;SCHLEGEL and JANNASCH, 1992) and mono-graphs (e.g., DIX and WEBSTER, 1995, pp.53–54, pp. 322–332). Elementary informationon this subject can be found in any textbook ofgeneral microbiology (e.g., LAMANNA andMALLETTE, 1959, pp. 422–444). Thus, there isno need here for a further discussion of thistopic.