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 obtain...

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Main Authors: Violetta La Cono, Erika Arcadi, Gina La Spada, Davide Barreca, Giuseppina Laganà, Ersilia Bellocco, Maurizio Catalfamo, Francesco Smedile, Enzo Messina, Laura Giuliano, Michail M. Yakimov
Format: Article
Language:English
Published: MDPI AG 2015-09-01
Series:Microorganisms
Subjects:
Online Access:http://www.mdpi.com/2076-2607/3/3/500
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spelling doaj-b6badc9b9a84439da934ed54688adce02020-11-24T22:32:25ZengMDPI AGMicroorganisms2076-26072015-09-013350051710.3390/microorganisms3030500microorganisms3030500A Three-Component Microbial Consortium from Deep-Sea Salt-Saturated Anoxic Lake Thetis Links Anaerobic Glycine Betaine Degradation with MethanogenesisVioletta La Cono0Erika Arcadi1Gina La Spada2Davide Barreca3Giuseppina Laganà4Ersilia Bellocco5Maurizio Catalfamo6Francesco Smedile7Enzo Messina8Laura Giuliano9Michail M. Yakimov10Institute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, ItalyInstitute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, ItalyInstitute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, ItalyDepartment of Organic and Biological Chemistry, University of Messina, Salita Sperone 31, Villaggio S. Agata, Messina 98166, ItalyDepartment of Organic and Biological Chemistry, University of Messina, Salita Sperone 31, Villaggio S. Agata, Messina 98166, ItalyDepartment of Organic and Biological Chemistry, University of Messina, Salita Sperone 31, Villaggio S. Agata, Messina 98166, ItalyInstitute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, ItalyInstitute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, ItalyInstitute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, ItalyInstitute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, ItalyInstitute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, ItalyMicrobial 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.http://www.mdpi.com/2076-2607/3/3/500deep-sea hypersaline anoxic lakesredoxiclineglycine betaine degradationmethylotrophic halophilesmethanogenesis
collection DOAJ
language English
format Article
sources DOAJ
author Violetta La Cono
Erika Arcadi
Gina La Spada
Davide Barreca
Giuseppina Laganà
Ersilia Bellocco
Maurizio Catalfamo
Francesco Smedile
Enzo Messina
Laura Giuliano
Michail M. Yakimov
spellingShingle Violetta La Cono
Erika Arcadi
Gina La Spada
Davide Barreca
Giuseppina Laganà
Ersilia Bellocco
Maurizio Catalfamo
Francesco Smedile
Enzo Messina
Laura Giuliano
Michail M. Yakimov
A Three-Component Microbial Consortium from Deep-Sea Salt-Saturated Anoxic Lake Thetis Links Anaerobic Glycine Betaine Degradation with Methanogenesis
Microorganisms
deep-sea hypersaline anoxic lakes
redoxicline
glycine betaine degradation
methylotrophic halophiles
methanogenesis
author_facet Violetta La Cono
Erika Arcadi
Gina La Spada
Davide Barreca
Giuseppina Laganà
Ersilia Bellocco
Maurizio Catalfamo
Francesco Smedile
Enzo Messina
Laura Giuliano
Michail M. Yakimov
author_sort Violetta La Cono
title A Three-Component Microbial Consortium from Deep-Sea Salt-Saturated Anoxic Lake Thetis Links Anaerobic Glycine Betaine Degradation with Methanogenesis
title_short A Three-Component Microbial Consortium from Deep-Sea Salt-Saturated Anoxic Lake Thetis Links Anaerobic Glycine Betaine Degradation with Methanogenesis
title_full A Three-Component Microbial Consortium from Deep-Sea Salt-Saturated Anoxic Lake Thetis Links Anaerobic Glycine Betaine Degradation with Methanogenesis
title_fullStr A Three-Component Microbial Consortium from Deep-Sea Salt-Saturated Anoxic Lake Thetis Links Anaerobic Glycine Betaine Degradation with Methanogenesis
title_full_unstemmed A Three-Component Microbial Consortium from Deep-Sea Salt-Saturated Anoxic Lake Thetis Links Anaerobic Glycine Betaine Degradation with Methanogenesis
title_sort three-component microbial consortium from deep-sea salt-saturated anoxic lake thetis links anaerobic glycine betaine degradation with methanogenesis
publisher MDPI AG
series Microorganisms
issn 2076-2607
publishDate 2015-09-01
description 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.
topic deep-sea hypersaline anoxic lakes
redoxicline
glycine betaine degradation
methylotrophic halophiles
methanogenesis
url http://www.mdpi.com/2076-2607/3/3/500
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