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Microorganisms. 2015 Sep 09;3(3):500-17. doi: 10.3390/microorganisms3030500.

A Three-Component Microbial Consortium from Deep-Sea Salt-Saturated Anoxic Lake Thetis Links Anaerobic Glycine Betaine Degradation with Methanogenesis.

Microorganisms

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

Affiliations

  1. Institute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, Italy. [email protected].
  2. Institute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, Italy. [email protected].
  3. Institute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, Italy. [email protected].
  4. Department of Organic and Biological Chemistry, University of Messina, Salita Sperone 31, Villaggio S. Agata, Messina 98166, Italy. [email protected].
  5. Department of Organic and Biological Chemistry, University of Messina, Salita Sperone 31, Villaggio S. Agata, Messina 98166, Italy. [email protected].
  6. Department of Organic and Biological Chemistry, University of Messina, Salita Sperone 31, Villaggio S. Agata, Messina 98166, Italy. [email protected].
  7. Institute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, Italy. [email protected].
  8. Institute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, Italy. [email protected].
  9. Institute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, Italy. [email protected].
  10. Institute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, Italy. [email protected].
  11. Mediterranean Science Commission (CIESM), 16 bd de Suisse, MC 98000, Monaco. [email protected].
  12. Institute for Coastal Marine Environment, CNR, Spianata S. Raineri 86, Messina 98122, Italy. [email protected].

PMID: 27682102 PMCID: PMC5023251 DOI: 10.3390/microorganisms3030500

Abstract

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.

Keywords: deep-sea hypersaline anoxic lakes; glycine betaine degradation; methanogenesis; methylotrophic halophiles; redoxicline

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