22 Anaerobic Metabolism and its Regulation
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1 22 Anaerobic Metabolism and its Regulation MICHAEL J. MCINERNEY Norman, OK, USA 1 Introduction Trophic Structure of Anaerobic Ecosystems Methanogens Physiology of Methanogens Effect of Sulfate on Methanogenesis Regulation of Fermentative Metabolism Regulation of Syntrophic Metabolism Environmental Factors Temperature Effect of ph and Volatile Acid Toxicity Types of Reactors Conventional Stirred Anaerobic Reactor Phase Separated Systems Fixed Film or Anaerobic Filter Reactors Fluidized/Expanded Bed Reactors Anaerobic Rotating Biological Contactor Anaerobic Baffle Reactor Upflow Anaerobic Sludge Blanket Reactor (UASB) Concluding Remarks References 472
2 Anaerobic Metabolism and its Regulation 1 Introduction Methanogenesis is an important terminal electron accepting process in many anaerobic environments where the supply of oxygen, nitrate, oxidized forms of sulfur, iron, and manganese are limited (FERRY, 1993). Examples of such environments include freshwater and some marine sediments, flooded soils, wet wood of trees, tundra, landfills, and sewage digestors. In these environments, a complex microbial community consisting of many interacting microbial species completely degrades natural polymers such as polysaccharides, proteins, nucleic acids, and lipids to methane and carbon dioxide. Because of the large amounts of organic matter that are degraded in the natural environments, methanogenesis is an important process in cycling of carbon and other elements in nature and may be responsible for up to 60% of atmospheric methane (CONRAD, 1996). The amount of energy released during methanogenesis is relatively low compared to other terminal electron accepting processes. For example, the conversion of hexoses to methane and carbon dioxide releases only 15% of the energy that would be released by the aerobic mineralization of hexose (SCHINK, 1997). Thus, the amount of biomass produced per unit of substrate degraded is much less than that of other terminal electron accepting processes. For this reason, methanogenesis has been used as the treatment of choice for sewage and other complex wastes since sludge yields are low and most of the energy in the original substrates is retained in the energyrich fuel, methane. Anaerobic digestion is often a net energy producer, resulting in significantly lower operating costs compared to aerobic treatment (LETTINGA, 1995). Although the low cell yields associated with anaerobic digestion make it attractive for wastewater treatment, it is also one of its main disadvantages because large reactor volumes and long retention times are needed to achieve the required treatment efficiency (MCCARTY, 1971). Thus, only relatively high strength wastes such as sewage are treated by anaerobic digestion. In addition, anaerobic digestion is often perceived as being an unstable process (ANDERSON et al., 1982; MCCARTY, 1971; SPEECE, 1983). However, great advances have been made in the past 20 years in our understanding of the biochemistry and energetics of anaerobic metabolism. This has allowed the delineation of the most sensitive steps in the process and the development of strategies to enhance the operational stability of anaerobic reactors. The result has been the development of novel reactors where the slow growing organisms are retained in the reactor even at high volume loadings. With these advances, it is now believed that almost any type of waste can be treated (LETTINGA, 1995). This chapter will provide a brief overview of the microbiology of anaerobic digestion and the factors that regulate this process. The constraints that thermodynamics places on key reactions will be discussed to illustrate its role in the control of the flow of carbon and energy during anaerobic digestion. In addition, the properties of microorganisms involved will be discussed to understand how population dynamics influences the process. There is a number of excellent reviews and books where these issues are treated in greater detail (DOLFING, 1988; FERRY, 1993; HOBSON et al., 1974; LETTINGA, 1995; LOWE et al., 1993; MALI- NA and POHLAND, 1992; MCCARTY and SMITH, 1986; MCINERNEY and BRYANT, 1981; SCHINK, 1988, 1997; SPEECE, 1983). 2 Trophic Structure of Anaerobic Ecosystems In anaerobic digestion, organic matter is completely degraded to methane and carbon dioxide in discrete steps by the concerted action of several different metabolic groups of microorganisms (Fig. 1) (MCINERNEY and BRYANT, 1981). In the first step, fermentative bacteria hydrolyze the polymeric substrates such as polysaccharides, proteins, and lipids and ferment the hydrolysis products to acetate and longer-chain fatty acids, CO 2, formate, H 2, NH 4c and HS P. Acetogeneic bacteria O-demethylate pectins and low molecular weight ligneous materials and ferment hydroxylated
3 2 Trophic Structure of Anaerobic Ecosystems 457 Fig. 1. Schematic representation of the different metabolic steps involved in the complete degradation of organic matter to methane and carbon dioxide (modified from MCINERNEY and BRYANT, 1981). and methoxylated aromatic compounds with the production of acetate (DOLFING, 1988). In the next step, a group of organisms, usually called syntrophic or proton reducing acetogenic bacteria, degrades propionate and longer-chain fatty acids, alcohols, and some amino acids and aromatic compounds to the methanogenic substrates, H 2, formate, and acetate. The degradation of these compounds with H 2 production is thermodynamically unfavorable unless the concentration of H 2 (or formate) is kept low by H 2 using bacteria such as methanogens (MCINERNEY and BRYANT, 1981). Because of the diverse number of organisms involved in these reactions and their ability to perform other types of metabolisms such as fermentation or sulfate reduction (SCHINK, 1997; MCINERNEY, 1992), the organisms that participate at this second step will be called syntrophic metabolizers. The final step involves two different groups of methanogens, the hydrogenotrophic methanogens which use the H 2 and formate produced by other bacteria to reduce CO 2 to CH 4 and the acetotrophic methanogens which metabolize acetate to CO 2 and CH 4. In the gastrointestinal tract of animals, organic matter is only partially converted to CO 2 and CH 4 (WOLIN, 1982). Acetate and longerchain fatty acids accumulate and are absorbed and used by the animal as energy sources. Only fermentative bacteria and H 2 or formate using methanogens seem to be involved in this partial methane fermentation. In termite guts (BREZNAK, 1994), the cecum of rodents and the large intestine of most humans (MILLER and WOLIN, 1994), the reduction of carbon dioxide to acetate by acetogenic bacteria seems to be the dominant electron accepting reaction. In these latter ecosystems, the community structure appears to be similar to that of the rumen, except that H 2 using acetogenic bacteria replace the H 2 using methanogens as the terminal electron accepting group. In ecosystems with high levels of sulfate, such as marine and estuarine sediments and petroleum reservoirs, sulfate reduction rather than methanogenesis is the terminal electron
4 Anaerobic Metabolism and its Regulation accepting reaction. Organic matter is completely oxidized to CO 2 with the reduction of sulfate to sulfide. Again, the degradation process involves the concerted efforts of several metabolic groups of bacteria with the sulfate reducing bacteria apparently performing the functions of the syntrophic metabolizers and the hydrogenotrophic and acetotrophic methanogens (MCINERNEY, 1986; OUDE ELFERINK et al., 1994; STAMS, 1994) since the degradation of propionate and longer-chain fatty acids to carbon dioxide in marine sediments does not require interspecies H 2 transfer (BANAT and NEDWELL, 1983). However, it is likely that the use of H 2 by sulfate reducers influences product formation of fermentative bacteria in a manner analogous to that found in methanogenic environments. This brief survey of the trophic structure of anaerobic ecosystems reveals that, in general, anaerobic metabolism proceeds in a stepwise manner where several metabolic groups of bacteria interact in the mineralization process. This is in contrast to metabolism under aerobic and denitrifying conditions where a single species is usually able to mineralize completely a compound when the electron acceptor (e.g., oxygen or nitrate) is in excess. The degree of mutual interdependence between the different trophic groups in anaerobic communities varies considerably depending on the genetic capabilities of the organisms and the constraints that kinetics and thermodynamics place on key reactions. For some interactions, energy limitations are such that neither partner can operate without the activity of the other organism. Perturbations may result in the accumulation of intermediates such as H 2 and acetate that exceed the narrow limits that are needed for the degradation of key intermediates such as fatty acids to be thermodynamically favorable. Other perturbations may stimulate fermentative metabolism or enhance the growth of certain fermentative populations, resulting in the production of acetate or other organic acids at rates faster than the other trophic groups can degrade these acids. Thus, the efficiency of anaerobic digestion will depend on the dynamics and kinetics of key populations within the reactor as well as on thermodynamic limitations. The challenge of anaerobic digestion is to maintain the appropriate balance between the different groups of bacteria so that rates of production of key intermediates match consumption rates and the pool sizes are and within the narrow limits that thermodynamics places on these reactions. 3 Methanogens 3.1 Physiology of Methanogens Methanogens are a taxonomically and phylogenetically diverse group of microorganisms (BOONE et al., 1993; JONES et al., 1987; ZINDER, 1993) that all gain energy for growth from the reactions that lead to the production of methane.as a group, methanogens use a small number of compounds, H 2 or one-carbon atom compounds (BOONE et al., 1993; ZINDER, 1993). This specialization makes methanogens dependent on other organisms for the supply of substrates in most anaerobic environments. Without methanogens, effective degradation of organic matter would cease due to the accumulation of nongaseous products of fermentation which have almost the same energy content as the original substrate. The ability of methanogens to use H 2 plays a key regulatory role that controls the types of products made by fermentative bacteria and sets the thermodynamic conditions required for the degradation of fatty and aromatic acids. The favorable thermodynamics of H 2 use by methanogens (Tab. 1) allows them to metabolize H 2 to very low partial pressures. Methanogens are able to metabolize H 2 down to H 2 partial pressures ranging from 3 7 Pa (LOVLEY, 1985; CORD-RUWISCH et al., 1988). Methanogens also have a high affinity for H 2 use, with apparent K M values in the range of 5 13 M (670 1,700 Pa) (Tab. 2) (ROBINSON and TIED- JE, 1984; WARD and WINFREY, 1985; ZINDER, 1993). With H 2 partial pressures ranging from 2 1,200 Pa in digestors (CORD-RUWISCH et al., 1997; GUWY et al., 1997; MOSEY and FERNAN- DEZ, 1989; STRONG and CORD-RUWISCH, 1995), this means that the methanogens are undersaturated with respect to H 2 use. Thus, in-
5 3 Methanogens 459 Tab. 1. Reactions Involved in Syntrophic Metabolism a Reaction G 0b [kj per reaction] Methanogenic reactions 4H 2 c HCO 3P c H c ] CH 4 c 3 H 2 O P135.6 Acetate P c H 2 O ] P CH 4 c HCO 3 P 31.0 Syntrophic reactions without H 2 use by methanogens Lactate P c 2H 2 O ] Acetate P c HCO 3P ch c c 2H 2 P 4.2 Ethanol c H 2 O ] Acetate P c H c c 2H 2 c 9.6 Butyrate P c2h 2 O ] 2 Acetate P c H c c 2 H 2 c 48.3 Propionate P c3h 2 O ] Acetate P c HCO 3P ch c c 3H 2 c 76.1 Benzoate P c 7H 2 O ] 3 Acetate P c HCO 3P c 3H c c 3H 2 c 70.6 b Acetate P c 4 H 2 O ] 2 HCO 3P c H c c4h 2 c104.6 Syntrophic reactions with H 2 use by methanogens 2 Lactate P c H 2 O ] 2 Acetate P c HCO 3P c CH 4 c H c P143.6 P 2 Ethanol chco 3 ] 2 Acetate P c H 2 OcH c c CH 4 P Butyrate P chco 3P c H 2 O ] 4 Acetate P c H c c CH 4 P Propionate P c 3 H 2 O ] 4 Acetate P c HCO 3P c H c c 3 CH 4 P Benzoate P c 19H 2 O ] 12 Acetate P c HCO 3P c 9H c c 3CH 4 P124.4 a Calculated from the data in THAUER et al. (1977). b Calculated using the free energy of formation for benzoate given in KAISER and HANSELMANN (1982). Tab. 2. Selected Kinetic Data for the Use of Hydrogen, Formate and Acetate by Methanogenic Bacteria Substrate Organisms Apparent K m Reference Threshold Reference Hydrogen most methano M KRISTIJANSSON et al Pa CORD-RUWISCH et al. gens (1982), ROBINSON (1988), LOVLEY (1985), and TIEDJE (1984) LOVLEY et al. (1984) Formate many methano M LOVLEY et al. (1984), M SCHAUER et al. (1982) gens SCHAUER et al. (1982) Acetate Methano mm SCHÖNHEIT et al mm WESTERMANN et al. sarcina sp. (1982), WESTERMANN (1989), FUKUZAKI et al. et al. (1989) (1990a) Methano- F mm HUSER et al. (1982), 5 75 M WESTERMANN et al. saeta sp MIN and ZINDER (1989), MIN and (1989), OHTSUBO ZINDER (1989), et al. (1992), AHRING AHRING and WESTERand WESTERMANN MANN (1987a), (1987a) JETTEN et al. (1990) creases in H 2 production may not result in higher H 2 partial pressures because the H 2 consumption rate by methanogens would also increase (KASPAR and WUHRMANN, 1978 a; ROBINSON and TIEDJE, 1982; SHEA et al., 1968; STRAYER and TIEDJE, 1978). Because of the large capacity for H 2 use by methanogens, H 2 concentrations are normally very low in welloperated anaerobic digestors, even though large amounts of H 2 are produced. As will be
6 Anaerobic Metabolism and its Regulation discussed in Sects. 4 and 5, the ability of methanogens to maintain low levels of H 2 affects the types of products formed by fermentative bacteria and is essential for the degradation of fatty and aromatic acids by syntrophic associations. Formate is a common fermentation product, especially by bacteria that use pyruvate formate lyase in their metabolism, and may be an essential intermediate for syntrophic metabolism (THIELE and ZEIKUS, 1988; DONG et al., 1994). Many methanogens are able to use formate and it serves as a source of electrons for methane formation equivalent to H 2. The affinity for formate use varies for different methanogens (Tab. 2).The apparent K M values for formate use was 5 26 M for two rumen methanogens, 580 M for Methanobacterium formicicum, and 0.22 mm for Methanospirillum hungatei (LOVLEY et al., 1984; SCHAUER et al., 1982). SCHAUER et al. (1982) reported that the lowest concentration of formate metabolized was 26 M for M. formicicum and 15 M for M. hungatei. Acetate is a major product of fermentative metabolism and is quantitatively the most important substrate for methane production. About 60 90% of the methane produced in anaerobic digestors are derived from the methyl group of acetate (BOONE, 1982; MACKIE and BRYANT, 1981; MOUNTFORT and ASHER, 1978; SMITH and MAH, 1966). At thermophilic temperatures or at high ammonium levels, the oxidation of the methyl group of acetate to H 2 may be the predominant route for acetate metabolism (see Sect. 5). Acetate using methanogens include members of the genera Methanosarcina and Methanosaeta (BOONE et al., 1993). Methanosarcina sp. have faster growth rates, higher apparent K M values for acetate use, and higher threshold acetate values than Methanosaeta sp. (Tab. 2) (ZINDER, 1993). The differences in the apparent K M values for acetate use have been attributed to differences in respective enzymes used to activate acetate (JETTEN et al., 1990). Since Methanosarcina sp. and Methanosaeta sp. have different threshold values for acetate use but use the same reaction for acetate metabolism (Tab. 1), the threshold values cannot represent a thermodynamic limitation. Acetate threshold values may result when a critical or inhibitory concentration of undissociated acetic acid is reached which, for Methanosarcinca sp., is between 4 and 7 M (FUKUZAKI et al., 1990a). Consistent with the known growth characteristics of the acetotrophic methanogens, a drop in acetate concentrations below 1 mm was correlated with a displacement of Methanosarcina sp. by Methanosaeta sp. in a thermophilic digestor (ZINDER et al., 1984). Generally, high-rate anaerobic sludge blanket reactors usually have granules composed of Methanosaeta sp. rather than Methanosarcina sp. (GROTENHUIS et al., 1991; WU et al., 1993). Interestingly, RASKIN et al. (1996) found that Methanosaeta sp. and Methanosarcina sp. were present at approximately equal levels in glucose degrading anaerobic biofilm reactors even though acetate levels were below the threshold values for Methanosarcina sp. The maintenance of Methanosarcina in these biofilms could not be attributed to the utilization of other substrates such as methanol, suggesting that there may be Methanosarcina sp. that have a lower threshold value than has been reported in the literature. STRAYER and TIEDJE (1978) found that acetate was converted to methane at or near the maximal rate in eutrophic lake sediments since the addition of acetate to these sediments did not result in a corresponding increase in the rate of acetate utilization or methane production. This suggests that there is little additional capacity to metabolize acetate if the acetate production rates increase. A similar conclusion was reached by HICKEY and SWITZENBAUM (1991) for anaerobic sewage digestors. This is probably the reason why acetate concentrations in digestors increase when organic or volume loading rates increase. Methanol, methylamine and trimethylamine also serve as substrates for Methanosarcina sp. and other methylotrophic methanogens (BOONE et al., 1993). These compounds may be important substrates for methanogenesis in marine systems (OREMLAND and POLCIN, 1982). Some hydrogenotrophic methanogens can oxidize secondary alcohols to ketones and primary alcohols to carboxylic acids (WIDDEL, 1986). Additional methanogenic substrates are discussed by ZINDER (1993) and BOONE et al. (1993).
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