Halorhabdus tiamatea: Proteogenomics and glycosidase activity measurements identify the first cultivated euryarchaeon from a deep-sea anoxic brine lake as potential polysaccharide degrader.

Johannes Werner, Manuel Ferrer, Gurvan Michel, Alexander J Mann, Sixing Huang, Silvia Juarez, Sergio Ciordia, Juan P Albar, Maria Alcaide, Violetta La Cono, Michail M Yakimov, André Antunes, Marco Taborda, Milton S da Costa, Tran Hai, Frank Oliver Glöckner, Olga V Golyshina, Peter N Golyshin, Hanno Teeling, The MAMBA consortium

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Abstract

Euryarchaea from the genus Halorhabdus have been found in hypersaline habitats worldwide, yet are represented by only two isolates: Halorhabdus utahensis AX-2T from the shallow Great Salt Lake of Utah, and Halorhabdus tiamatea SARL4BT from the Shaban deep-sea hypersaline anoxic lake (DHAL) in the Red Sea. We sequenced the H. tiamatea genome to elucidate its niche adaptations. Among sequenced archaea, H. tiamatea features the highest number of glycoside hydrolases, the majority of which were expressed in proteome experiments. Annotations and glycosidase activity measurements suggested an adaptation towards recalcitrant algal and plant-derived hemicelluloses. Glycosidase activities were higher at 2% than at 0% or 5% oxygen, supporting a preference for low-oxygen conditions. Likewise, proteomics indicated quinone-mediated electron transport at 2% oxygen, but a notable stress response at 5% oxygen. Halorhabdus tiamatea furthermore encodes proteins characteristic for thermophiles and light-dependent enzymes (e.g. bacteriorhodopsin), suggesting that H. tiamatea evolution was mostly not governed by a cold, dark, anoxic deep-sea habitat. Using enrichment and metagenomics, we could demonstrate presence of similar glycoside hydrolase-rich Halorhabdus members in the Mediterranean DHAL Medee, which supports that Halorhabdus species can occupy a distinct niche as polysaccharide degraders in hypersaline environments.
Original languageEnglish
Pages (from-to)2525-2537
Number of pages13
JournalEnvironmental Microbiology
Volume16
Issue number8
Early online date15 Jan 2014
DOIs
Publication statusPublished - Aug 2014

Keywords

  • Adaptation, Physiological
  • Anaerobiosis/physiology
  • Biological Evolution
  • Ecosystem
  • Enzyme Assays
  • Genome, Archaeal
  • Glycoside Hydrolases/genetics
  • Halobacteriaceae/classification
  • Indian Ocean
  • Lakes/microbiology
  • Metagenomics
  • Oxygen/metabolism
  • Phylogeny
  • Polysaccharides/metabolism
  • Salt Tolerance/genetics
  • Sodium Chloride
  • Utah
  • Water Microbiology

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    Werner, J., Ferrer, M., Michel, G., Mann, A. J., Huang, S., Juarez, S., Ciordia, S., Albar, J. P., Alcaide, M., La Cono, V., Yakimov, M. M., Antunes, A., Taborda, M., da Costa, M. S., Hai, T., Glöckner, F. O., Golyshina, O. V., Golyshin, P. N., Teeling, H., & MAMBA consortium, T. (2014). Halorhabdus tiamatea: Proteogenomics and glycosidase activity measurements identify the first cultivated euryarchaeon from a deep-sea anoxic brine lake as potential polysaccharide degrader. Environmental Microbiology, 16(8), 2525-2537. https://doi.org/10.1111/1462-2920.12393