Taxonomy and ecology of methanogens

1 FEMS Microbiology Reviews 87 (1990) Pubfished by Elsevier 297 FEMSRE Taxonomy a ecology of methanogens J.L. Garcia Laboratoire de Microbiologie ORST...

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FEMS Microbiology Reviews 87 (1990) 297-308 Pubfished by Elsevier

297

FEMSRE 00180

Taxonomy and ecology of methanogens J.L. Garcia Laboratoire de Microbiologie ORSTOM, Université de Provence, Marseille, France

Key words: Methanogens; Archaebacteria; Taxonomy; Ecology 1. INTRODUCTION

More fhan nine reviews on taxonomy of methanogens have been published during the last decade [l-91, after the discovery of the unique biochemical and genetic properties of these organisms led to the concept of Archaebacteria at the end of the seventies. Moreover, important economic factors have ,placed these bacteria in the limelight [ 5 ] , including the need to develop alternative forms of energy, xenobiotic pollution control, the enhancement of meat yields in the cattle industry, the distinction between biological and thermocatalytic petroleum generation, and the global distribution of methane in the earth's atmosphere.

2. TAXONOMY OF METHANOGENS The methanogenic bacteria all fulfill a common physiological purpose, which is to produce methane as one of the final products of energy metabolism. Among the 68 species described up to now, 77% are hydrogenotrophs, 14%acetotrophs, and 28% methylotrophs, among which ten species are obligate methylotrophs. Only 3% of the species use H2 to reduce methanol to methane. An as yet indeterminate number of alcoholotrophs can form

Correspondence to: J.L. Garcia, Laboratoire de Microbiologie ORSTOM, Université de Provence, 3 Place Victor-Hugo, 13331 Marseille, Cedex 3, France.

methane from CO2 using alcohols as hydrogen donors; 2-propanol is oxidized to acetone, and 2-butanol to 2-butanone. Carbon monoxide may also be converted into methane; most hydrogenotrophic species (60%) will also use formate. Some aceticlastic species are incapable of oxidizing H,. The aceticlastic species of the genus Methanosurcina are the most metabolically diverse methanogens, whereas the obligate aceticlastic Methanosaeta (Methanothrix) can use only acetate. The taxonomy of the methanogenic bacteria has been extensively revised in the light of new information based on comparative studies of 16 S rRNA oligonucleotide sequences, membrane lipid composition, and antigenic fingerprinting data. The phenotypic characteristics often do not provide a sufficient means of distinguishing among taxa or determining the phylogenetic position of a taxon. Recently, Boone and Whitman [lo] have proposed minimal standards for describing new taxa of methanogens, which have been approved by the Subcommittee for Taxonomy of Methanogenic Bacteria) The characteristics of methanogens have been summarized in the recent review by Oremland [ 5 ] . Since the fundamental study by Balch et al. [l], the taxonomy of methanogens has yielded a classification including three orders, seven families and twenty genera; 68 species have been 'described, not all of which have yet been validated by the International List of Bacteria (TaSle 1). The order Methanobacteriales contains all the methanogens with pseudomurein cell walls; C,, and C,, isopranyl glycerol ethers are abundant in

0168-6445/90/$03.50 O 1990 Federation of European Microbiological Societies

298

Table 1 Characteristics of methanogenic bacteria Organism

Morphology -~ Shape

Dimensions (P.m)

Order Methanobacteriales Fam. Methaiiobacteriaceae Methanobacterium alcaliphiluni bryantii espaiiolae formicicuin iuaiiovii pahistre thkrmoaggregans thernioalcaliphihan thernioatttotrophicimi therinoforinicicum iiligiiiosuin wolfei , Methanobrevibacter arboriphilus riiininantiitm sniithii Methanosphaera cuniculi : stadtinanae Fam. Methanothermaceae Methanothennus feruidics sociabilis Order Methanococcales Fam. Methanococcaceae Methanococcus aeolicus deltae halophilus jannaschii inaripaludis therniolithotrophicus vannielii uoltae Order Methanomicrobiales Fam. Methanoinicrobiaceae Methanomicrobium mobile Methanolacinia paynteri Methanospirilluin hungatei Methanogenium aniiltu bourgense , cariaci

‘Gram reaction

+ + + + + -

Motility

Optimum growth conditions

PH

Temp. (OC?

NaCl (M?

8.1-9.1 6.9-7.2 5.6-6.2 6.6-7.8 7.0-7.4 7.0 7.0-7.5 7.5-8.5 7.2-7.6 7.0-8.0 6.0-8.5 7.0-7.7

37 37-39 35 37-45 45 37 65 58-62 65-70 45-60 37-40 55-65

nd nd nd nd nd < 0.3 O nd nd nd nd <1.7

7.8-8.0

neutral neutral

30-37 37-39 37-39

nd nd nd

6.8 6.5-6.9

35-40 37

nd nd

6.5 6.5

83 88

nd nd

nd nd 6.5-7.4 5-7 6.5-8.0 6.5-8.0 7.0-9.0 6.5-8.0

nd 37 26-36 85 35-40 65 35-40 35-40

nd O. 6-0.7 1.0-1.7 0.3-0.7 0.2-0.6 0.3-0.7 0.1 0.2-0.6

rod rod rod rod rod rod rod rod rod rod rod rod

0.5-0.6 X 2-25 0.5-1.0 X 10-15 0.8 X 3-22 0.4-0.8 X2-15 0.5-0.8 X1.2 0.5 X 2.5-5 0.4 X 4-8 0.3 X 3-4 0.4-0.6 X 3-120 0.3-0.6 X 2-120 0.2-0.6 X 2-4 0.4X 2.4-2.7

coccobacillus coccobacillus coccobacillus

0.5 X 1.3 0.7 X 0.8-1.7 0.5-0.7 X1.0-1.5

coccus coccus

0.6-1.2 1.0

rod rod

0.3-0.4 X 1-3 0.3-0.4 X 3-5

irregular coccus irregular coccus irregular coccus irregular coccus irregular coccus irregular coccus irregular coccus irregular coccus

nd 1.0-1.5 0.5-2.0 1.o 1.0 1.o 1.0 1.5

nd nd

curved rod

0.7 X 1.5-2.0

-

6.1-6.9

40

nd

irregular rod

0.6 X 1.5-2.5

-

6.6-7.2

40

0.15

sheathed spiral

0.4 X7.4-10

-

nd

30-37

nd

irregular coccus irregular coccus irregular coccus

1-2 < 2.6

6.3-6.8 6.2-6.6

35-42 20-25

0.5

-

+ + + i-

+ + +

+

+

+ i-.

nd nd nd nd

-

-

-

-

< 0.18

299

Table 1 (continued) Organism c

Morphology Shape

I

(pm)

' e'

,

Dimensions

frittonii limiatans marisnigri olentangyi organophilum tationis thermophilicuni Fam. Methanocorpusculaceae Methanocorpusculum aggregans bauaricum Iabreunum parvuin sinense Fam. Methanoplanacene Methanoplanus endosymbiosus limicola Fam. Methanosurcinue Methanosarcina acetiuorans alcaliphilum barkeri frisia mazei thermophila vacuolata Methanolobus Siciliae tindarius Vulcani Methanococcoides euhalobius nietliylutetis Methanohalophilus mahii zhilinae Methanohalobium euestigatus Halomethanococcus Alcaliphilum doii Meihanosaeta concilii thermoacetophila Methanothrix soehngenii Methanopyrus

irregular coccus irregular coccus irregular coccus irregular coccus irregular coccus irregular coccus irregular coccus

1-2.5 1.5

< 1.3 1-1.5 0.5-1.5 3 1.0-1.4

Gram reaction

Motility

-

-

-

irregular coccus irregular coccus irregular coccus irregular coccus irregular coccus

0.5-2.0

irregular disk plate

0.5-1 X 1.6-3 0.1-0.3 X 1.5-2.0 -

(1.0 0.4-2.0 0.5-1.0 X1.0

pseudosarcina, coccoid pseudosarcina pseudosarcina pseudosarcina, coccoid pseudosarcina, coccoid pseudosarcina pseudosarcina irregular coccus irregular coccus irregular coccus

0.8-1.2 0.8-1.2 0.8-1.2

-

irregular coccus irregular coccus

1-2.5 1-3

-

irregular coccus irregular coccus

0.5-2.5 0.8-1.5

-

+

Optimum growth conditions PH

Temp. ("'2)

NaCl (M)

7.0-7.5 7.0 6.8-7.3

O O 0.1

nd 6.4-7.3 7.0 6.5-7.2

57 40 20-25 37 30-35 37-40 55-60

0.2 0.3 < 0.3 0-0.3

6.4-7.2 7.0 7.0 6.8-7.5 7.0

35-37 37 37 37 30

< 0.18 nd 0-0.2 0-0.8 O

6.6-7.1

neutral

32 40

0.25 0.1-1.0

'

1.5-2.5

-

6.5 -7.5

35-40

0.2

1.5-2.0

+

neutral

30-40

nd

0.5-2.0

-

6.5-7.2

36

0.3-0.7

1.0-3.0 1.5-2.5 1-2

+

7.0-7.2 6.0 7.5

30-40 50 40

nd nd nd

nd 6.5 nd

37 37 31

nd 0.5 nd

6.8-7.3

neutral

28-37 30-35

1.o 0.2-0.6

-

7.4-7.5 9.2

35-37 45

1.0-2.5 0.5-1.0

+ +

-

-

4-

irregular coccus irregular coccus irregular coccus

3.3-1.5

-

6.8

35-37

1.8-3.6

sheathed rod sheathed rod

0.8-1.2X0.3 1.0-1.2X5

-

7.1-7.5 6.5

35-40 60

nd nd

sheathed rod sheathed rod

0.8-1.2 X 2-3 0.5 x 8-10

7.4-7.8 6.5

35-40 98

nd 0.25

4-

300 Table 1 - Continued Organism

Use of substrates H2 CO2

+

Order Methanobacteriales Fam. Methanobacteriaceae Methanobacterium alcaliphiluni bryantii espaiiodae formicicuni ivanovii palustre thermoaggregans thernioalcaliphilum tliermoaictotropRicum thermoformicicum uliginosiim wolfei Methanobrevibacter arboriphilus rimiinantium sinithii Methanosphaera cuniculi stadtmanae Fam. Methanotherïnaceae Methanothermus feruidus sociabilis Order Methanococcales Fam. Methanococcaceae Methanococcus aeoliciis deltae halophilus jannaschii maripaludis thermolithotrophicus uannielii ooltae Order Methkomicrobiales Fam. Methanomicrobiaceae Methanomicrobium mobile Methanolacinia paynteri MethanospiriIIum hungatei , Methanageniuni anuius bourgense cariaci friitonii liminatans marisnigri

Formate

Acetate

Methyl compounds

Alcoq

Prototrophy

hols

DNA G + C content (mol%)

Refs. Y 1

/

+ + + + + f + + + + + + + + + -

-

++ -

-

+ -

-

+

+

-

-

-

-

-

-

-

-

-

-

-

nd nd -

-

-

-

-

-

-

23 26

25 26

nd nd

+ +

33-34 33-34

21 28

-

40.5 38 31 33 34 33 30

29 30 31 32 33 34 35 I

nd

-

49

36

+ +/-

-

45

37,38

+

45-49

39,40

nd

-

-

-

-

-

+

59 50-52 49.2 59-60 51-62

41 42 43 44 45 43

-

-

-

+

nd nd

-

-

+ + +

-

-

+

+ +

-

23 24 1

nd nd

-

-

28-32 31 28-31

-

f

-

+ -

-

-

+ + +

nd

,

11 12 13 14 15 16 .17 18 19 20 21 22

-

-

+ + + + +

+ + + f. + + + +

51 33-38 33 38-42 36.6 34 42 38.8 48-52 43 29-34 61

-

-

+

-

nd

nd

-

-

nd

+ +/+

-

-

-

+

i-

+ + + i4-

+ -

301 Table 1 (continued)

Organism

Use of substrates H2 CO2

ir

+

I

Formate

Acetate

'-1

b

5

J

olentaiigyi organophiluni tationis tlierniophilicuni Fam. Methanocorpusculaceae Methanocorpusculum aggregaiis bavaricum labreanuni parvum sinense Fam. Methanoplaiiaceae Methanoplanus endosynibiosus liinicola Fam. Methanosarcinae Methanosarcina acetworam alcaliphiluni barkeri frisia niazei therinophila vacuolata Methanolobus siciliae tindarius vulcani Methanococcoides eulialobius niethyhtens Methanohalophilus mahii zhilitiae Methanohalobium evestigatus Halomethanococcus alcaliphiluni doii Methanosaeta concilii thermoacetophila Meihanothrix soehngenii Meihanopyrus

Methyl compounds

AlCo-

Prototrophy

DNAGSC content

Refs.

hols

(mol%)

nd

54.4 46.7 54 56-60

30 46 47 48,49

52 47.7 50 48 52

50,51 52 53 54 52

nd

-

39 48

55 56,57

nd

41

58 59 60 61,62 63 64,65 66

4-

-

+/nd

+

nd

+-

nd nd nd nd

-

39-51 38 42 42 36-51

-

41 46 39

. 67

nd nd

43 42

69 70

nd nd

49 38

71 72

nd

nd

73

nd

43.2

74 75

nd nd

61 nd

16-79 79,80

nd nd

52 60

81 82

68 67

nd: not determined.

I$

all the species tested. None of the species described are motile. The order Methanococcales contains one genus with abundant C,, isopranyl I

glycerol ethers, but C,, ethers are absent except in M. jannaschii. All of the species are irregular cocci, which are almost motile by a polar tuft of flagella

302

with proteinaceous cell walls. The order Methanomicrobiales shows various morphologies: small rods, spirilla, highly irregular cocci, sarcina and unusual irregular flattened plates. The cell walls are proteinaceous and the lipids include both C,, and C40 or only C,, isopranyl glycerol ethers. The thermophilic methanogen, strain TAM [83] is a filamentous ro'd able to utilize H,-CO, and formate, as well as acetate. Methanoplasma elizabethii [84] is an unusual species that lacks a cell wall. The taxonomic classification of these organisms has mt yet been established. ,

3. ECOLOGY OF METHANOGENS

The distribution of methanogens in natural environments is highly dependent on their adaptation to various temperature, pH and salinity ranges. The thermophilic species, which amount to 20% of the total known methanogens, include only six genera. Most methanogens grow within a relatively narrow pH range (6.0-&O), and two species of the genus Methanobacterium have been reported as alkaliphilic methanogens with an optimum pH of between 8 and 9 [11,18], and Methanohalophdus zhilinae, a halophilic, methylotrophic methmogen with an optimum pH of 9.2 [721. 3.1. Methanogenic interactions In natural anaerobic habitats containing complex organic compounds, where light, sulfate, and nitrate are limited, the methanogenic bacteria cooperate with other chemo-heterotrophic bacteria in degrading organic substrates. The ultimate formation of methane and CO, marks the last step in a series of dissimilatory reactions by which organic compounds are completely degraded. Methanogens can use H,-CO,, formate, or acetate directly produced by fermentative bacteria, or in an obligate association named syntrophy, with obligate hydrogen producing acetogenic bacteria. The latter phenomenon was termed 'interspecies hydrogen transfer' [85]. Five genera of syntrophic bacteria have been described as #partnershipsof methanogens, contributing to the

oxidation of fatty acids, benzoic acid, or fructose. In the absence of a hydrogen scavenger, these reactions are endergonic and cannot develop. When H, is consumed, the reaction becomes exergonic and the syntroph can grow and oxidize the substrate. Interspecies hydrogen transfer has also been demonstrated with defined cocultures of methanogens with non-syntrophic anaerobic bacteria and even a rumen anaerobic fungus. Other mechanisms have been proposed to account for coupling syntrophic methanogenesis: interspecies bicarbonate-formate transfer during conversion of ethanol or lactate [86], and interspecies acetate transfer during degradation of acetone [87]. Mineral terminal electron acceptors such as nitrate or sulfate inhibit methanogenesis in sediments or digesters by channeling electron flow to thermodynamically more efficient bacteria such as denitrifiers or sulfate reducers [88,89] that have higher affinity to H, and higher growth yields [90-921. Methanogenesis and sulfate reduction are not always mutually exclusive and occur simultaneously, when methane is produced from methanol and/or methylated amines, substrates for which sulfate reducers show little affinity [93,94]. In ecosystems where no organic material is present, methan-ogenesis occurs from geochemical hydrogen evolved from hot springs, for instance. In this case methanbgens act as the primary producers. '

3.2. Natural habitats of methanogenic bacteria 3.2.1. Soil, aquatic environments, digestors. Rice field soils are similar to the littoral of lakes and are characterized by the presence of plants and the occurrence of oxic and anoxic zones in the sediment. The aerenchyme and intracellular space system of rice plants mediate the transport of CH, from the anoxic sediment into the atmosphere [95]. In the absence of plants, CH, is released almost exclusively by the emission of bubbles. In planted soils, up to 80% of the methane produced does not reach the atmosphere but is oxidized in the rizosphere [96]. CH4 oxidation has also been detected in the oxic surface layer of submerged paddy soil. Methanogenesis is strongly inhibited by brackish water in these soils [96,97]. Several strains of nitrogen fixing Methanobacterium and

303

Metlianosarcina have been isolated from rice soils [981. Many workers have illustrated the importance of acetate as a methane precursor in both freshwaters and marine sediments [89,99,100], and demonstrated that H, is a rate limiting factor in the process of methanogenesis in sediments [90,101-1031. Landfills constitute another type of habitat from which methanogens have been isolated [104]. It has been shown that strictly anaerobic bacteria form the dominant population in digesters, and that methanogens accounted for about 10% of the total microflora [105-108]. Dolfing and Bloemen [lo91 have presented a rapid and reliable method for assessing the potential specific activity of methanogenic sludge. Enzyme-linked immunosorbent assay (ELISA method-llO), and immunologic analysis methods [ l l l ] have been used for detecting and quantifying methanogens in digesters or mixed cultures. 3.2.2. Extreme environments. Thermophilic environments, such as hot springs, solfataras or submarine hydrothermal vents, are sites of active methanogenesis. Only a few species of hyperthermophilic methanogens have been isolated [27,32, 821. Biogenic methane has also been detected in hypersaline environments. The patterns and rates of methane production in hypersaline algal mats may depend on a complex interaction between salinity, the use of methylated amines for osmoregulation by algae, and the formation of TMA during fermentation [112]. All the species isolated up to now are methylotrophic methanogens belonging to newly described genera [71-751. Studies are in progress with sediments from a hypersaline lake in Senegal, containing 350 81-1 salt (Ollivier, personal communication). 3.2.3. Within living organisms. Methanogens are directly involved in the digestive processes of ruminants and other animals including insects. Since the work of Hungate, the activities of methanogenic bacteria in the rumen and the cecum of herbivorous mammals have become well known. Little methane production from acetate occurs here because the animals absorb the volatile fatty acids produced during the fermentation process

through the intestinal epithelium. Thus, about 82% of the CH, formed in the rumen comes from H, reduction of CO,, while about 18%is derived from formate [113]. However, methylotrophic methanogens are present, and participate in methanogenesis from methylamines or methanol. Methanogens are also present in the large bowel of humans. The most prominent species of methanogens belong to the genus Methaizobrevibacter [114], but Methanosphaera [115] and Methanogenium [115,116] strains can also be encountered. The same bacteria have been detected in the oral cavity of humans, being associated with dental plaque [117]. Methanogens have also been identified in the gut of various insects including termites, the gut microflora of which contains about 10% of methanogens [118]. The contribution of termites to atmospheric methane has given rise to some controversy during the last decade [119,120], and has been estimated at 2-5 X lo’, g per year. The heartwood tissues of trees can become infected with soil bacteria and develop conditions for methanogenesis at the expense of the degradation of cellulose and pectins [121]. Methanobrevibacter arboriplzilus has been isolated from this habitat [23]. Methanogens have also been found to be endosymbionts of protozoa, removing the hydrogen produced by the protozoa via interspecies hydrogen transfer [56,122,123]. In the oceans, methane evolution results from the activities of methanogens located within the intestinal tracts of marine animals (plankton and fishes [124]), as well as in the forestomachs of baleen whales [125] where fermentation of chitin occurs in a situation analogous to that of rumen in ruminants. 3.2.4. Atmospheric methane. The global tropospheric methane concentrations average about 1.6 ppm, and a two- to threefold increase has occurred over the past 100-200 years [126], with a present increase of 2% per year. Because methane absorbs in the infrared, it plays an analogous role to that of carbon dioxide (‘Greenhouse’ effect). In addition, it is destroyed in the atmosphere by reacting with hydroxyl radicals, resulting in the production of carbon monoxide and hydrogen [127]. However, methane may react with chlorine

304

or nitrous oxide, derived from chlorofluorocarbons and fertilizer applications respectively, and help protect the stratospheric ozone layer from being destroyed by these compounds [128]. The residence time of methane in the atmosphere is now thought to be about 8 years [129].

NOTE ADDED IN PROOF After completion of the manuscript, publications appeared on the following topics: Description ‘of a new species of Methanohalophilus : Liu, Y., Boone, D.R. and Choy, C. (1990) Methanohalophilus oregonense sp.nov., a methylotrophic methanogen from an alkaline, saline aquifer. Int. J. Syst. Bacteriol. 40, 111-116. Transfer of several species of genus Methanogenium to the new genus Methanoculleus :Maestrojuan, G.M., Boone, D.R., Xun, L., Mah, R.A. and Zhang, L. (1990) Transfer of Methanogenium bourgense, Methanogenium m arisn igri, Methan ogen ium olentangyi, and Methanogenium thernzophilicum to the genus Methanoculleus gen.nov., emendation of Methanoculleus marisnigri and Methanogenium and d,escription of new strains of Methanoculleus bourgense and Methanoculleus marisnigri. Int. J. Syst. Bacteriol. 40, 117-122. Existence of family Methanoplanaceae contradicted by 116s sequencing data. Genus Halomethanococcus not clearly distinguished from Methanohalophilus. Methanococcus deltae subjective synonym of Methanococcus maripaludis. Methanococczis halophilus unassigned strain of Methanohalobizim : Boone, D.R. (1990) Catalog of the Oregon Collection of methanogens. Oregon Graduate Institute of Science and Technology, Beaverton, Oregon, pp. 52.

REFERENCES [I] Balch, W.E., Fox, G.E., M a g ” , L.J., Woese, C.R. and Wolfe, R.S. (1979) Methanogens: reevaluation of a unique biological group. Microbiol. Rev. 43, 260-296. [2] Reference omitted. [3] Jones, W.J., Nagle, D.P., Jr. and Whitman, W.B. (1987) Methanogens and the diversity of archaebacteria. Microbiol. Rev. 51, 135-177.

[4] Mah, R.A. and Smith, M.R. (1981) v e methanogenic bacteria, in The Procaryotes. A Handbook on Habitats, Isolation and Identification of Bacteria, Vol. 1 (Starr, M.P., Stolp, H., Triiper, H.G., Balows, A. and Schlegel, H.G., Eds.), pp. 948-977, Springer-Verlag, Berlin. [5] Oremland, R.S. (1988) Biogeochemistry of methanogenic bacteria, in Anaerobic Bacteria (Zehnder, A.J.B., Ed.), pp. 641-705, J o b Wiley & Sops, New York. [6] Taylor, G.T. (1982) The methanogenic bacteria. Progr. Ind. Microbiol. 16, 231-329. [7] Whitman, W.B. (1985) Methanogenic bacteria, in Bacteria-a Treatise on Structune and Function, Vol. VI11 Archaebacteria, pp. 3-84, Academic Press, Orlando. [SI Zehnder, A.J.B., Ingvorsen, K. and Marti, T. (1982) Microbiology of methane bacteria, in Anaerobic Digestion 1981 (Hugues, D.E., Stafford, D.A., Wheatley, B.I., Baader, W., Letting, G., Nyns, E.J., Verstraete, W. and Wentvirorth, R.L., Eds.), pp. 45:68, Elsevier Biomedical Press, New York. [9] Boone, D.R. and Mah, R.A. (1989) Methanogenic archaebacteria, in Bergey’s Manual of Systematic Bacteriology (Staley, J.T., Bryant, M.R., Pfennig, N. and Holt, J.G., Eds.), Vol. 3, pp. 2173-2216, Williams & Wilkins, Baltimore. [lo] Boone, D.R. and Whitman, W.B. (1989) Proposal of minimal standards for describing newi taxa of methanogenic bacteria. Int. J. Syst. Bacteriol. 38, 212-219. [ l l ] Worakit, S., Boone, D.R., Mah, R.A., AbdeNamie, M.E. and El-Halwagi, M.M. (1986) Methanobacterium alcalzphilum sp. nov., an H,-utilizing methanogen that grows at high pH values. Imt. J. Srst. Bacteriol. 36, 380-382. [12] Boone, D.R. (1987) Replacement of the type strain of Methanobactenuni formimum, and reinstatement of Methanobacterium bryantii sp. nov., nom.rev. (ex Balch and Wolfe, 1981) with M.0.H. (DSM 863) as the type strain. Int. J. Syst. Bacteriol. 37, 172-173. [13] Patel, G.B,, Sprott, G.D. and Fein, J.E. (1990) Isolation and characterization of Methanobacterrum espanolae sp. nov., a mesophilic, moderately acidiphilic methanogen. Int. J. Syst. Bacteriol. 40, 12-18. [14] Bryant, M.P. and Boone, D.R. (1987) Isolation and characterization of Methanobacterium formleicum MF. Int. J. Syst. Bacteriol. 37, 171. [15] Jain, M.K., Thompson, T.E., Conway de Macario, E. and Zeikus, J.G. (1987) Speciation of Methanobacterium strain Ivanov as Methanobacterium luanouil, sp. nov. System. Appl. Microbiol. 9, 77-82. [16] Zellner, G., Bleicher, K., Braun, E., Kneifel, H., Tindall, B.J., Conway de Macario, E. and Winter, J. (1989) Characterization of a new mesophilic, secondary alcoholutilizing methanogen, Methanobacterium palifitre, spec. nov. from a peat bog. Arch. MicrobioP. 151, 1-9. [17] Blotevogel, K.H. end Fischer, U. (1985) Isolation and characterizatìon of a new themophikc and autotrophic methane producing bacterium: Methanobacterium thermoaggregans spec. nov. Arch. Microbiol. 142, 218-222.

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v d n 1

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