A Three-Component Microbial Consortium from Deep-Sea Salt-Saturated Anoxic Lake Thetis Links Anaerobic Glycine Betaine Degradation with Methanogenesis.
Microbial communities inhabiting the deep-sea salt-saturated anoxic lakes of the Eastern Mediterranean operate under harsh physical-chemical conditions that are incompatible with the lifestyle of common marine microorganisms. Here, we investigated a stable three-component microbial consortium obtained from the brine of the recently discovered deep-sea salt-saturated Lake Thetis. The trophic network of this consortium, established at salinities up to 240, relies on fermentative decomposition of common osmoprotectant glycine betaine (GB). Similarly to known extreme halophilic anaerobic GB-degrading enrichments, the initial step of GB degradation starts with its reductive cleavage to trimethylamine and acetate, carried out by the fermenting member of the Thetis enrichment, Halobacteroides lacunaris TB21. In contrast to acetate, which cannot be easily oxidized in salt-saturated anoxic environments, trimethylamine represents an advantageous C₁-substrate for methylotrophic methanogenic member of the Thetis enrichment, Methanohalophilus sp. TA21. This second member of the consortium likely produces hydrogen via methylotrophic modification of reductive acetyl-CoA pathway because the initial anaerobic GB cleavage reaction requires the consumption of reducing equivalents. Ecophysiological role of the third member of the Thetis consortium, Halanaerobium sp. TB24, which lacks the capability of either GB or trimethylamine degradation, remains yet to be elucidated. As it is true for cultivated members of family Halanaerobiaceae, the isolate TB24 can obtain energy primarily by fermenting simple sugars and producing hydrogen as one of the end products. Hence, by consuming of TB21 and TA21 metabolites, Halanaerobium sp. TB24 can be an additional provider of reducing equivalents required for reductive degradation of GB. Description of the Thetis GB-degrading consortium indicated that anaerobic degradation of osmoregulatory molecules may play important role in the overall turnover of organic carbon in anoxic hypersaline biotopes.
Institute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, Italy. violetta.lacono@iamc.cnr.it.
Violetta La
VL
Cono
Institute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, Italy. eren@tiscali.it.
Erika
E
Arcadi
Institute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, Italy. gina.laspada@iamc.cnr.it.
Gina La
GL
Spada
Department of Organic and Biological Chemistry, University of Messina, Salita Sperone 31, Villaggio S. Agata, Messina 98166, Italy. dbarreca@unime.it.
Davide
D
Barreca
Department of Organic and Biological Chemistry, University of Messina, Salita Sperone 31, Villaggio S. Agata, Messina 98166, Italy. giuseppina.lagana@unime.it.
Giuseppina
G
Laganà
Department of Organic and Biological Chemistry, University of Messina, Salita Sperone 31, Villaggio S. Agata, Messina 98166, Italy. ersiliasanta.belocco@unime.it.
Ersilia
E
Bellocco
Institute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, Italy. maurizio.catalfamo@iamc.cnr.it.
Maurizio
M
Catalfamo
Institute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, Italy. francesco.smedile@iamc.cnr.it.
Francesco
F
Smedile
Institute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, Italy. enzo.messina@iamc.cnr.it.
Enzo
E
Messina
Institute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, Italy. laura.giuliano@iamc.cnr.it.|Mediterranean Science Commission (CIESM), 16 bd de Suisse, MC 98000, Monaco. laura.giuliano@iamc.cnr.it.
Laura
L
Giuliano
Institute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, Italy. michail.yakimov@iamc.cnr.it.
Michail M
MM
Yakimov
deep-sea hypersaline anoxic lakes; glycine betaine degradation; methanogenesis; methylotrophic halophiles; redoxicline
Environ Microbiol. 2011 Aug;13(8):1908-23
21054738
Appl Environ Microbiol. 2004 Jul;70(7):4411-4
15240332
Appl Environ Microbiol. 2010 Apr;76(7):2129-35
20118363
Nucleic Acids Res. 2004 Feb 25;32(4):1363-71
14985472
FEMS Microbiol Lett. 2012 May;330(1):1-9
22339687
Archaea. 2010 Dec 23;2010:690737
21234345
Orig Life Evol Biosph. 2007 Apr;37(2):177-88
17136435
Int J Food Microbiol. 2008 May 10;124(1):21-6
18403036
Mol Biol Evol. 2011 Oct;28(10):2731-9
21546353
Sci Rep. 2013 Dec 19;3:3554
24352146
Antonie Van Leeuwenhoek. 2011 Nov;100(4):639-53
21751028
ISME J. 2007 Dec;1(8):743-55
18059497
Int J Syst Bacteriol. 1999 Jan;49 Pt 1:103-12
10028251
Nature. 2006 Mar 9;440(7081):203-7
16525471
Proc Natl Acad Sci U S A. 2009 Jun 9;106(23):9151-6
19470485
Syst Appl Microbiol. 1999 Sep;22(3):434-44
10553296
J Bacteriol. 1990 Feb;172(2):762-70
1688842
Anaerobe. 1995 Aug;1(4):185-99
16887527
Appl Environ Microbiol. 1988 Jan;54(1):130-136
16347519
Environ Microbiol. 2012 Jan;14(1):268-81
22040283
Extremophiles. 2003 Feb;7(1):29-34
12579377
Environ Microbiol. 2007 Mar;9(3):801-13
17298378
Int J Syst Evol Microbiol. 2007 May;57(Pt 5):1035-40
17473254
FEMS Microbiol Lett. 1995 Dec 1;134(1):115-9
8593948
Appl Environ Microbiol. 2003 May;69(5):2631-7
12732531
PLoS One. 2012;7(3):e33439
22479398
Int J Syst Evol Microbiol. 2008 Jan;58(Pt 1):215-20
18175711
Appl Environ Microbiol. 1992 Jan;58(1):260-6
16348626
Nucleic Acids Res. 2007;35(21):7188-96
17947321
Environ Microbiol. 2011 Aug;13(8):2250-68
21518212
Environ Microbiol. 2014 Aug;16(8):2525-37
24428220
Antonie Van Leeuwenhoek. 1990 Nov;58(4):291-8
2082817
Environ Microbiol. 2015 Feb;17(2):364-82
25622758
Nucleic Acids Res. 1997 Sep 1;25(17):3389-402
9254694
Syst Appl Microbiol. 2012 Sep;35(6):368-73
22817877