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Reclassification of Methanogenium Tationis and Methanogenium Liminatans As Methanofollis Tationis Gen. Nov., Comb. Now and Methanofollis Lirninatans Comb

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Reclassification of Methanogenium Tationis and Methanogenium Liminatans As Methanofollis Tationis Gen. Nov., Comb. Now and Methanofollis Lirninatans Comb international Journal of Systematic Bacteriology (1999), 49, 247-255 Printed in Great Britain Reclassification of Methanogenium tationis and Methanogenium liminatans as Methanofollis tationis gen. nov., comb. now and Methanofollis lirninatans comb. nov. and description of a new strain of Methanofollis liminatans Gerhard Zellner,’ David R. Boone,’ Jyoti Ke~wani,~William B. Whitman,3 Carl R. W~ese,~Anja Hagelstein,’ B. J. Tindal15 and Erko Stackebrandt’ Author for correspondence : Gerhard Zellner. Tel: + 49 89 3 187 2579. Fax : + 49 89 3 187 3361. e-mail : [email protected] 1 Institute of Hydrology, Sequencing of 165 rRNA genes and phylogenetic analysis of Methanogenium GSF National Research - tationis DSM 2702T(OCM 433 (T = type strain) and Methanogenium liminatans Center for Environment and Health, Ingolstadter GKZPZT (= DSM 41403 as well as other members of the family LandstraBe 1, D-85764 Methanomicrobiaceae revealed that both species belong to a separate line of Neuherberg, descent within this family. In addition, a new strain of Methanogenium Germany liminatans, strain BM1 (= DSM 10196), was isolated from a butyrate- * Oregon Graduate Institute degrading, fluidized bed reactor and characterized. Cells of both species are of Science and Technology, Portland, OR 97291 -1000, mesophilic, highly irregular cocci that use HJCO, and formate for growth and USA methanogenesis. In addition, Methanogenium liminatans strains GKZPZT and 3 Department of BMI used 2-propanol/C02, 2-butanol/C02 and cyclopentanol/CO,. Both species Microbiology, University of contained diether and tetraether lipids. The polar lipids comprised amino- Georgia, 527 Biological phosphopentanetetrol derivatives, which appear to be characteristic Iipids Sciences Building, Athens, GA 30602-2605, USA within the family Methanomicrobiaceae. The pattern of glycolipids, phosphoglycolipids and amino-phosphoglycolipids was consistent with the 4 Department of M icro bio I ogy, U n iversity of assignment of these two species to a taxon within the family Illinois, Urbana, IL 61801, Methanomicrobiaceae, but also permitted them to be distinguished from USA other higher taxa within this family. The G+C contents of the DNA of 5 DSMZ - Deutsche Methanogenium tationis and Methanogenium liminatans were 54 and Sammlung von 60 mol0h (T, and HPLC), respectively. On the basis of the data presented, the Mikroorganismen und Zellkulturen, D-38124 transfer of Methanogenium tationis and Methanogenium liminatans to the Braunschweig, Germany genus Methanofollis gen. nov. as Methanofollis tationis comb. nov. and Methanofollis liminatans comb. nov., respectively, is proposed, with Methanofollis tationis as the type species. Keywords : Methanogeniuni tationis, Methanogenium lirninatans, Methanofollis gen. nov., lipids, phylogeny INTRODUCTION indicates a wide evolutionary diversity among these methanogenic Archaea. However, only a limited num- The DNA of irregularly coccoid methanogens has a ber of phenotypic characteristics of irregularly coccoid wide range of G+C contents (38-61 mol%), which methanogens are available for taxonomic purposes. In addition to morphology and substrate spectrum, et ,. , . , . , , , , ., . , . .. , . , .. , . .. ,, , .. .. .. .. ., , .. , .. .. .. ., . .. .. .. .. .. .. .. .. characteristics such as polyamine content (Zellner Abbreviations: PAS, periodic acid-Schiff; UASB, upflow anaerobic sludge al., 1989a; Blotevogel et al., 1991 ; Boone et al., 1993), blanket. cellular lipids (Grant et al., 1985; Zellner et al., The CenBanWEMBL accession numbers for the 165 rDNA and rRNA se- 1989a, b, c; Blotevogel et al., 1991 ; Koga et al., 1993) quences reported in this paper are Y16428, Y16429, AF095266-AF095272. and whole-cell protein patterns (Maestrojuan et al., ~ ~~ ~ 00846 0 1999 IUMS 247 G. Zellner and others 1990) have been used. The S-layer architecture and the cultures, isolation procedures and cultivation of Methano- apparent molecular mass of glycopro tein subunits genium liminatans strains. WHP medium was based on the have also been used (Zellner et al., 1989a, c, 1990; recipe described by Zellner & Jargon (1997) except that yeast Messner & Sleytr, 1992; Sleytr et al., 1993). Due to the extract, peptone and additional sodium sulfate were omitted. WHP medium contained 1 pM sodium tungstate and was fact that few physiological tests can be used to used for the cultivation of strains DSM 2702T,GKZPZT and differentiate taxa within the methanogenic Archaea, BM 1. Substrates (e.g. sodium formate, sodium acetate, 2- other phenotypic characters (e.g. cell wall structure, propanol, 2-butanol, cyclopentanol) were added from an- chemical composition, polyamines) and genotypic aerobic, sterile stock solutions (207'0, w/v or v/v) as characters (e.g. 16s rDNA sequence) must be used to indicated to give concentrations of 0.5 YO(w/v or v/v) in the delineate the higher taxonomic ranks. Recent serum bottles. Cells were grown under H,/CO, (4: 1, v/v, developments in the taxonomy of both Archaea and 300 kPa) in 120ml serum bottles on a rotary shaker Bacteria indicate that this combination of phenotypic (150 r.p.m.). When other substrates were used instead of and genotypic methods is suitable for the delineation hydrogen, N,/CO, (4: 1, v/v, 300 kPa) served as the gas at- of taxa in a system which seeks to base these on the mosphere. For the preparation of large masses of cells, cells were grown in H,/CO, (4: 1, v/v) at a flow rate of 50 1 h-l in phyletic groupings detected by such data. a 12 1 fermenter (Biostat S; Braun). Analysis of the sequences of 16s rRNA or its genes Methanogenium tationis was grown as described previously revealed a high diversity of irregularly coccoid meth- (Zabel et al., 1984). Methanoculleus olentangyi and anogenic strains, with some deeply rooted lines of Methanoculleus bourgensis were grown as described by descent in phylogenetic trees (Zellner et al., 1989a; Corder et al. (1983) and Ollivier et al. (1986), respectively. Rouviere et al., 1992; Boone et al., 1993). As a Methanocorpusculum labreanum was grown as described by consequence, several coccoid methanogens were re- Zhao et al. (1989). Methanocorpusculum sinense and classified on the basis of DNA-DNA hybridization Methanocorpusculum bavaricum were grown as described by studies and/or 16s rDNA sequence analysis (Xun et Zellner et al. (1989a). al., 1989; Zellner et al., 1989c; Maestrojuan et al., Source and habitat of strain BMI. Strain BM1 (= DSM 1990; Boone et al., 1993). This resulted in the descrip- 10 196) was isolated from a butyrate-degrading, fluidized bed tion of the five current genera of hydrogenotrophic, reactor inoculated with a culture originally derived from the irregularly coccoid methanogens of the order upflow anaerobic sludge blanket (UASB) reactor from the Met hanom icrobiales 1 Methanogen ium, Methanocul- wastewater treatment plant at a sugar refinery in Bruhl, leus, Methan olacin ia, Met hanoplan us and Met hanocor- Germany (Zellner et al., 1991). The predominant pusculum. methanogen in this bioreactor was an autofluorescent irregular coccus, similar in appearance to the new isolate Recently, the reclassification of Methanogenium (strain BM 1) described here, and several other methanogens tationis (Zabel et al., 1984) as Methanofollis tationis were identified immunologically (Zellner et al., 1991, 1997). was suggested (Boone et al., 1993) but not formally Enrichment and isolation of strain BM1. WHP medium with proposed. In this paper, the transfer of Methanogenium H,/CO, (4: 1, v/v, 300 kPa) as substrate was inoculated with tationis and Methanogenium liminatans as Methano- 1 YO(v/v) bioreactor liquid and incubated at 37 "C. The gas follis tationis gen. nov., comb. nov. and Methanofollis phase was regularly replaced and autofluorescent, irregularly liminatans comb. nov. is proposed on the basis of 16s coccoid cells increased in number simultaneously with the rDNA sequencing and chemotaxonomic and physio- formation of methane. This enriched culture was serially logical data. In addition, the isolation and charac- diluted into WHP medium and the highest dilution showing terization of a new Methanofollis liminatans strain, growth of the fluorescent, irregularly coccoid cells was again serially diluted. Aliquots (0.1 ml) of the dilutions were then BM1, is reported. streaked on agar plates with WHP medium plus 2.5 % (w/v) Oxoid agar (Unipath). All manipulations were performed in METHODS an anaerobic chamber (M. Braun) under a nitrogen at- mosphere. The plates were transferred into a stainless steel Reference strains. Methanogenium tationis strain (DSM anaerobic jar, pressurized to 300 kPa with H,/CO, (4: 1, 2702T) was obtained from the Deutsche Sammlung von v/v) and incubated at 37 "C. After 20 d incubation, the gas Mikroorganismen und Zellkulturen (DSMZ, Braunschweig, pressure had dropped to 150 kPa, indicating gas consump- Germany). Methanogenium liminatans strain GKZPZ' (= tion. The anaerobic jar was transferred into the anaerobic DSM 4140T) was isolated and (after deposition in the chamber. Cells were picked with a syringe needle from a DSMZ) subcultured in this laboratory. The newly isolated well-isolated colony, injected into a 120 ml serum bottle strain BMl has been deposited at the DSMZ as DSM 10196. containing 20 ml WHP medium under H,/CO, (4: 1, v/v, The following strains were obtained from the Oregon : 300 kPa) and incubated at 37 "C. This procedure resulted in Collection of Methanogens (Beaverton, OR, USA) the isolation of strain BM 1. Methanoculleus olentangyi RC/ER' (OCM
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