Nanohaloarchaea as beneficiaries of xylan degradation by haloarchaea

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  • Violetta La Cono
    Institute of Polar Research, Messina
  • Enzo Messina
    National Council of Research, CNR, Rome
  • Olga Reva
    University of Pretoria
  • Francisco Smedile
    Institute of Polar Research, Messina
  • Gina La Spada
    Institute of Polar Research, Messina
  • Francesca Crisafi
    Institute of Polar Research, Messina
  • Laura Marturano
    Institute of Polar Research, Messina
  • Noa Miguez
    CSIC, Madrid
  • Manuel Ferrer
    CSIC, Madrid
  • Elena A. Selivanova
    Russian Academy of Sciences
  • Olga Golyshina
  • Peter Golyshin
  • Manfred Rohde
    Helmholtz Centre for Infection Research, Braunschweig
  • Mart Krupovic
    Université Paris Cité,
  • Alexander Y. Merkel
    Russian Academy of Sciences
  • Dimitry Y. Sorokin
    Russian Academy of Sciences
  • John E. Hallsworth
    Queen's University, Belfast
  • Mikhail Yakimov
    Institute of Polar Research, Messina
AbstractClimate change, desertification, salinisation of soils and the changing hydrology of the Earth are creating or modifying microbial habitats at all scales including the oceans, saline groundwaters and brine lakes. In environments that are saline or hypersaline, the biodegradation of recalcitrant plant and animal polysaccharides can be inhibited by salt‐induced microbial stress and/or by limitation of the metabolic capabilities of halophilic microbes. We recently demonstrated that the chitinolytic haloarchaeon Halomicrobium can serve as the host for an ectosymbiont, nanohaloarchaeon ‘Candidatus Nanohalobium constans’. Here, we consider whether nanohaloarchaea can benefit from the haloarchaea‐mediated degradation of xylan, a major hemicellulose component of wood. Using samples of natural evaporitic brines and anthropogenic solar salterns, we describe genome‐inferred trophic relations in two extremely halophilic xylan‐degrading three‐member consortia. We succeeded in genome assembly and closure for all members of both xylan‐degrading cultures and elucidated the respective food chains within these consortia. We provide evidence that ectosymbiontic nanohaloarchaea is an active ecophysiological component of extremely halophilic xylan‐degrading communities (although by proxy) in hypersaline environments. In each consortium, nanohaloarchaea occur as ectosymbionts of Haloferax, which in turn act as scavenger of oligosaccharides produced by xylan‐hydrolysing Halorhabdus. We further obtained and characterised the nanohaloarchaea–host associations using microscopy, multi‐omics and cultivation approaches. The current study also doubled culturable nanohaloarchaeal symbionts and demonstrated that these enigmatic nano‐sized archaea can be readily isolated in binary co‐cultures using an appropriate enrichment strategy. We discuss the implications of xylan degradation by halophiles in biotechnology and for the United Nation's Sustainable Development Goals.

Keywords

  • Ecosystem, Haloferax, Xylans
Original languageEnglish
Pages (from-to)1803-1822
Number of pages20
JournalMicrobial Biotechnology
Volume16
Issue number9
Early online date14 Jun 2023
DOIs
Publication statusPublished - Sept 2023

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