2 Microbiology of Composting

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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
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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 Organic Wastes as Nutrients Water Availability Structure, Oxygen Supply and Aeration Temperature Hydrogen Ion Concentration, ph 48 5 Laboratory Composting 49 6 The Microorganisms of Composting The Main Groups of Microbes Active in Composting Bacteria Actinomycetes Fungi Microbial Successions in Composting 65 7 Hygienic Aspects of Composting Inactivation of Pathogens Emission of Microorganisms from Composting Plants 72 8 Phytopathogenic Aspects of Composting Inactivation of Plant Pathogens during Composting Adverse Effects of Fresh, Immature Compost on Plant Growth Control of Soilborne Plant Pathogens by Compost Control of Foliar Diseases by Compost Water Extracts 78 9 Balancing the Composting Process Mass Balance Energy Balance and Heat Transfer Heat Recovery from Composting Plants Mathematical Modeling of the Composting Process Odor Formation and Control Compost Maturity References 90 36 2 Microbiology of Composting List of Abbreviations APPL CFU GC HDMF MS PVC SAR TMV TOC v.s. acid precipitable, polymeric lignin colony forming unit gas liquid chromatography 3-hydroxy-4,5-dimethyl-2(5H)-furanone mass spectroscopy polyvinyl chloride systemic acquired resistance tobacco mosaic virus total organic compound volatile solids 1 Introduction In his comprehensive monographs, HAUG (1980, 1993) defines composting as the biological decomposition and stabilization of organic substrates under conditions which allow development of thermophilic temperatures as a result of biologically produced heat, with a final product sufficiently stable for storage and application to land without adverse environmental effects. This definition differentiates composting from the mineralization of dead organic matter taking place in nature above the soil or in its upper layers leading to a more or less complete decomposition besides the formation of humic substances; it thus describes the compost pile as a man-made microbial ecosystem. Composting has been carried out for centuries, originally as an agricultural and horticultural practice to recycle plant nutrients and to increase soil fertility (HOWARD, 1948); nowadays it has become also part of the management of waste disposal to get rid of the huge amounts of diverse organic waste produced by our civilized urban life. In most cases, the product compost has to be regarded as a by-product which hardly finances its production now often being carried out in highly mechanized plants (FINSTEIN et al., 1986; FIN- STEIN, 1992; JACKSON et al., 1992; STEGMANN, 1996). Composting has frequently been regarded as more an art than a science; this view, however, ignores the fact that its scientific base is well understood; of course, successful application of the principles requires experience as is more or less true for all applied sciences. In fact, the basic rules of composting have been known for decades as can be seen from numerous reviews and monographs of the last 25 years, beginning with UPDEGRAFF (1972) and ending with DE BERTOLDI et al. (1996). These surveys also indicate the broad interest of scientists of various disciplines in this process, 2 Heat Production by Microorganisms 37 disciplines such as agriculture, horticulture, mushroom science, soil science, microbiology and sanitary engineering. The literature on composting is vast, comprising numerous broad reviews and minireviews of which only few can be cited in addition to those mentioned above: GASSER (1985), BIDDLESTONE et al. (1987), MA- THUR (1991), MILLER (1991, 1993), HOITINK and KEENER (1993) and SMITH (1993); in addition, there exist also specific journals devoted solely or primarily to the subject, e.g., Compost Science, Agricultural Wastes, Müll & Abfall. Being well aware of the literature covered in these reviews, the author has tried to avoid repetition as much as possible; thus only selected papers will be considered, in addition to paying regard to some older work not reviewed until now because of its hidden publication. This review is primarily concerned with the microbiology of composting. However, since composting touches many related disciplines, even the restriction to this selected field has to take various aspects into consideration which may seem at first glance rather remote from the composting process per se: (1) The microbiology of self-heating of moist, damp organic matter has first been extensively studied in the case of agricultural products, e.g., hay, grain and wool. This phenomenon very early led to the concept of heat generation as part of microbial (and organismic in general) metabolism. (2) The microbiology of composting is somehow related to soil microbiology and litter decomposition, i.e., soil fertility, turnover of organic matter in nature and formation of humic substances. (3) The control of pathogenic agents in wastes to be composted, and the emission of pathogenic agents from compost plants are of concern to medical microbiologists. This aspect has to be extended to agents causing plant diseases and to the effect of compost on plant pathogens. (4) Mushroom cultivation includes the preparation of a compost substrate, a special process whose study contributed much to the general understanding of composting. The main focus of this chapter will be the compost pile as a microbial ecosystem, and a more proper title for it would be A Microbiologist s View of Composting. Most of the reviews cited above also deal with the microbiology of composting, and there are several which specifically discuss this aspect, e.g., FINSTEIN and MORRIS (1975) and LACEY (1980). Many papers mentioned there will not be cited in this review, and it is hoped that their authors will have some understanding for this approach: a reviewer has to make a selection of topics and of the literature to be cited, which inevitably leads to a somewhat personal view, not entirely free of bias. 2 Heat Production by Microorganisms Any metabolism from microbes to man leads inevitably to the production of heat (Fig. 1, Tab. 1). This is actually a consequence of the 2nd law of thermodynamics, i.e., only part of the energy consumed can be transformed into useful work, e.g., biosynthesis, while the rest is liberated as heat to increase the entropy of the surroundings. Very often, mostly just for simplification, the degradation of a carbohydrate (e.g., glucose) serves as an example to demonstrate this context: Tab. 2 gives an energy balance for the aerobic metabolism of 2 M glucose, assuming that 1 of them enters the energy metabolism producing 38 ATP M 1 glucose, whereas the other supplies the precursors for the biosynthesis of new biomass which consumes the 38 ATP: According to this calculation, which follows the reasoning of DIEKERT (1997), the catabolism has a physiological efficiency of 61 69%, whereas the anabolism of only 40%. A very similar balance has been found by TERROINE and WURMSER (1922) for the mold Aspergillus niger as discussed in detail by BATTLEY (1987, pp. 108ff): 59% of the energy (not weight!) of the glucose consumed were incorporated into new biomass (mycelium), whereas 41% were liberated as heat. 38 2 Microbiology of Composting O2 CO2 + H2O % (?) Flow to catabolism 40% as heat Energy content of all nutrients utilized 60% in ATP % (?) Flow to anabolism 40% (a) for formation of monomers (b) for formation of polymers (c) for other cell activities 60% as heat Energy content of produced biomass Fig. 1. Energy flow in aerobic metabolism of bacteria (for further explanation see text and Tab. 1). Tab. 1. Energy flow in Microorganisms with Glucose as Substrate: Proportioning of the Substrate Energy to New Biomass and Liberated Heat as well as especially the Y ATP Value Depend on the Number of ATP per Mol Glucose % Glucose Utilized for % Substrate Energy in Catabolism Anabolism New Liberated ATP Y s Y ATP (Energy (Biosyn- Biomass Heat Glucose 1 Production) thesis) A B B C C Tab. 2. Energy Balance of the Aerobic Metabolism of Glucose by Bacteria (Free Energy of Hydrolysis ATPcH 2 O ] ADPcP i : Ap52 kj, Bp46 kj) Metabolism A B Catabolic metabolism C 6 H 12 O 6 c6 O 2 ] 6 CO 2 c6 H 2 O G 0 1 pp2,872 kj Invested into 38 ATP (38 52 or 46 kj) G 0 1 pp1,976 kjp69% 1,748 kjp61% Liberated as heat G 0 1 pp1,896 kjp31% 1,124 kjp39% Anabolic metabolism Free energy of hydrolysis of 38 ATP G 0 1 pp1,976 kj Invested in biosynthesis, transport, movement G 0 1 pp1,790 kjp40% 1,699 kjp40% Liberated as heat G 0 1 pp1,186 kjp60% 1,049 kjp60% Total balance 2 M glucose (2 2,872) G 0 1 pp5,744 kj Liberated as heat G 0 1 pp2,082 kjp36% 2,173 kjp38% Fixed in new biomass G 0 1 pp3,662 kjp64% 3,571 kjp62% Note that the heat of combustion of 1 M glucose amounts to H c pp2,816 kj. 2 Heat Production by Microorganisms 39 The percentages of the substrate (1) employed for energy formation (catabolism) and (2) utilized for biosynthesis depend on the energy 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: One third of the substrate (glucose) is used for the production of ATP, whereas two thirds [more correctly 4 of the 6 carbon atoms (Eq. 1)] appear in the biomass; this results in an Y s of about 0.5 and an Y ATP of about 10 (Tab. 3). The heat produced in the metabolism of microbes cultivated on a small scale is rapidly dissipated to the environment and hardly noticed in laboratory experiments. Therefore, this phenomenon, although of great theoretical importance, is surprisingly not discussed in most textbooks of microbiology, a rare exception being the one by LAMANNA and MALLETTE (1959, pp ). Of course, heat production is of great practical significance in the mass culture of microorganisms and, therefore, treated in books on biochemical engineering, e.g., BAILY and OLLIS (1977, pp ) and CRUEGER and CRUEGER (1984, pp ); it has been extensively discussed by LUONG and Tab. 3. Equations of Microbial Growth Calculated for Various Growth Efficiencies (1) C 6 H 12 O 6 c0.8 NH 3 c2.0 O 2 ] 0.8 [C 5 H 7 O 2 N]c2.0 CO 2 c4.4 H 2 O Y s p90.4/180p0.502 (2) C 6 H 12 O 6 c0.7 NH 3 c2.5 O 2 ] 0.7 [C 5 H 7 O 2 N]c2.5 CO 2 c4.6 H 2 O Y s p79.1/180p0.430 (3) C 6 H 12 O 6 c0.6 NH 3 c3.0 O 2 ] 0.6 [C 5 H 7 O 2 N]c3.0 CO 2 c4.8 H 2 O Y s p67.8/180p0.376 (4) C 6 H 12 O 6 c0.5 NH 3 c3.5 O 2 ] 0.5 [C 5 H 7 O 2 N]c3.5 CO 2 c5.0 H 2 O Y s p56.5/180p0.314 (5) C 6 H 12 O 6 c0.4 NH 3 c4.0 O 2 ] 0.4 [C 5 H 7 O 2 N]c4.0 CO 2 c5.2 H 2 O Y s p45.2/180p0.251 (6) C 6 H 12 O 6 c0.3 NH 3 c4.5 O 2 ] 0.3 [C 5 H 7 O 2 N]c4.5 CO 2 c5.4 H 2 O Y s p33.9/180p0.188 (7) C 6 H 12 O 6 c0.2 NH 3 c5.0 O 2 ] 0.2 [C 5 H 7 O 2 N]c5.0 CO 2 c5.6 H 2 O Y s p22.6/180p0.125 HAUG (1993, p. 248) considered Y s p as a typical growth yield in composting; for Y s p0.1 he presented the following balance (here reduced to one mole of glucose). (8) C 6 H 12 O 6 c0.16 NH 3 c5.2 O 2 ] 0.16 [C 5 H 7 O 2 N]c5.2 CO 2 c5.7 H 2 O Y s p18.8/180p Note: Calculation in g (NB p New Biomass) (a) Complete oxidation of glucose without production of biomass 100 g glucosec106,7 g O 2 ] g CO 2 c60 g H 2 O (b) Eqs. (1) and (6) from above in g: Y s p0.502 : [100c7.5] substratec35.6 O 2 ] 50.2 NBc48.9 CO 2 c44.0 H 2 O Y s p0.188 : [100c2.8] substratec80.0 O 2 ] 18.8 NBc110.0 CO 2 c54.0 H 2 O (c) The following equation has been used for the hypothetical composting process discussed in Sect. 9 (Fig. 15 and Tab. 15, Equ. 8a Y s p : [100c3.02] substratec78.22 ] NBc CO 2 c53.6 H 2 O 2. Note Calculation of oxygen consumption in relation to loss of volatile solids, v.s., in g: Y s p0.502: v.s.p107.5p50.2p57.3c35.6 O 2 ] 48.9 CO 2 c44.0 H 2 O v.s. : 100c62.13 O 2 ]85.34 CO 2 c76.79 H 2 O Y s p0.188: v.s.p102.8p18.8p84.0c80.0 O 2 ] CO 2 c54.0 H 2 O v.s. : 100c95.23 O 2 ] CO 2 c64.28 H 2 O Y s p0.167: v.s.p102.5p16.7p85.8c83.0 O 2 ] CO 2 c54.7 H 2 O v.s. : 100c96.73 O 2 ] CO 2 c63.75 H 2 O 40 2 Microbiology of Composting VOLESKY (1983), in the monograph by BATT- LEY (1987) and in Vol. 1 of the Second Edition of Biotechnology by POSTEN and COONEY (1993, pp ). 3 The Phases of the Composting Process If the heat produced by the metabolism of microorganisms is prevented by some kind of insulation from being dissipated to the environment, the temperature of the habitat increases. This is the case when damp organic matter is collected in bulky heaps or kept in tight containers, as it is done when organic waste is composted either in large piles (windrows) or in boxes of various kinds. If the composting process is carried out as a batch culture as opposed to a continuous operation it proceeds in various more or less distinct phases which are recognized superficially by the stages of temperature rise and decline (Fig. 2). These temperature phases are, of course, only the reflection of the activities of successive microbial populations performing the degradation of increasingly more recalcitrant organic matter. As shown in Fig. 2, the time temperature course of the composting process can be divided into 4 phases: (1) During the first phase a diverse population of mesophilic bacteria and fungi proliferates, degrading primarily the readily available nutrients and thereby raising the temperature to about 45 C. At this point their activities cease, the vegetative cells and hyphae die and eventually lyse, and only heat resistant spores survive. (2) After a short lag period (not always discernible) there occurs a second more or less steep rise of temperature. This second phase is characterized by the development of a thermophilic microbial population comprising some bacterial species, actinomycetes and fungi. The temperature optimum of these microorganisms is between 50 and 65 C, their activities terminate at C. (3) The third phase can be regarded as a stationary period without significant changes of temperature because microbial heat production and heat dissipation balance each other. The microbial population continues to consist of thermophilic bacteria, actinomycetes, and fungi. (4) The fourth phase is characterized by a gradual temperature decline; it is best described as the maturation phase of the composting process. Mesophilic microorganisms having survived the high temperature phase or invading the cooling down material from the outside succeed the thermophilic ones and extend the degradation process as far as it is intended. Fig. 2 presents just one of numerous examples of the temperature course that can be found in the literature, very typical ones having been published by CARLYLE and NORMAN (1941), WALKER and HARRISON (1960), NIESE (1959). In all cases the 4 phases mentioned have been observed more or less distinctly leaving no doubt that they characterize very closely the composting process. Since the optimum temperature for composting is regarded to be about C, measures are being taken to prevent further self-heating except for a rather short period up to 70 C to guarantee the elimination of pathogens (see Sect. 7.1). However, 70 C appears to be not the limit of microbial heat production which can easily reach 80 C as practised in the Beltsville process (see Sect. 4.3). Under certain conditions even much higher temperatures leading to ignition can be reached, but neither the exact requirements for such an event nor the mechanism of ignition appear to be well understood (BOWES, 1984). Whereas there are only rare cases of self-ignition of manure piles or compost heaps (JAMES et al., 1928), this phenomenon is not uncommon in the storage of damp hay (GLATHE, 1959, 1960; CURRIE and FESTENSTEIN, 1971; HUSSAIN, 1972) and fat contaminated pie wool (WALKER and WIL- LIAMSON, 1957). 3 The Phases of the Composting Process 41 Fig. 2. Temperature course during the composting of urban garbage: four phases, mesophilic, thermophilic, stationary, and maturation, can easily be recognized (from PÖPEL, 1971). As mentioned above the temperature phases are just a reflection of the activities of successive microbial populations. This has been demonstrated by various means besides by a detailed analysis of the bacterial, actinomycete and fungal population: (1) Fig. 3, taken from NIESE (1969), shows that the microbial community of fresh refuse plus sewage sludge exhibits a respiratory activity only at 28 and 38 C, i.e., it consists primarily of mesophiles. On the contrary, the samples taken from the self-heated material started instantaneously to take up oxygen when incubated at 58 and 48 C; the relatively high respiration rate at 38 C is probably due to the broad temperature range of several thermophiles (Sect. 6, Fig. 8, Tab. 9). (2) Fig. 4, taken from FERTIG (1981), illustrates the O 2 uptake and CO 2 production during the temperature course of composting: 4 maxima of microbial activity can be observed, surprisingly within the very short time of 54 h. Two or three maxima of CO 2 evolution during composting have been observed by numerous authors, e.g., SIKORA et al. (1983) who discussed also earlier observations of this kind; VIEL et al. (1987) reported three maxima of oxygen consumption. (3) Finally, a detailed analysis of adaptation and succession of microbial populations in composting of sewage sludge has been undertaken by MCKINLEY and VESTAL (1984, 1985a,b), the main aim of their study being to ascertain the optimal temperature for the composting process: The microbial communities from hotter samples were better adapted to higher temperatures than those from cooler samples and vice versa, as 42 2 Microbiology of Composting 4 The Compost Pile as a Microbial Habitat Fig. 3a,b. Oxygen uptake of microbial communities in Warburg flasks at different temperatures: A fresh garbage plus sewage sludge, B composting material removed from the pile during the high temperature phase, 28 C 38 C 48 C 58 C (according to NIESE, 1969). shown by the determination of the rate of [ 14 C]-acetate incorporation into cellular lipids and calculation of its apparent energies of activation and inactivation. Lipid phosphate was used as indicator of viable bacterial biomass. The authors came to the conclusion, that the composting temperature should not be allowed to exceed 55 C in agreement with numerous other investigators. In order to secure fast stabilization of the waste material, the microorganisms performing this task have to be provided with nutrients, water and oxygen. Of course, the demand for nutrients appears to be contradictory since material without nutrients does not need to be stabilized. However, because organic waste material in any case lends itself to decomposition the nutritional state of the starting material deserves consideration. A fourth parameter of composting is the temperature, which plays actually a dual role in this habitat: It is the result of microbial activity without necessity of being taken care of at the commencement of the process and at the same time it is a selective agent determining the microbial population at any stage of the composting process, eventually demanding its regulation by technical measures. Finally, the ph of the habitat can be considered as environmental factor. It is obvious that the various parameters are intimately related; this should be kept in mind when in Sects they are necessarily treated separately. 4.1 Organic Wastes as Nutrients Waste suitable for composting comes from very diverse sources: grass clippings, leaves, hedge cuttings, food remains, fruit and vegetables waste from the food industry, residues from the fermentation industry, solid and liquid manure from animal houses, wastes from the forest, wood and paper industries, rumen contents from slaughtered cattle and sewage sludge from wastewater treatment plants. Thus, the starting material of composting varies tremendously in its coarse composition, and in addition there is often a seasona
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