Nanohaloarchaea as beneficiaries of xylan degradation by haloarchaea

Author:

La Cono Violetta1ORCID,Messina Enzo2ORCID,Reva Oleg3ORCID,Smedile Francesco1ORCID,La Spada Gina1ORCID,Crisafi Francesca1ORCID,Marturano Laura1,Miguez Noa4,Ferrer Manuel4ORCID,Selivanova Elena A.5ORCID,Golyshina Olga V.6ORCID,Golyshin Peter N.6ORCID,Rohde Manfred7ORCID,Krupovic Mart8ORCID,Merkel Alexander Y.9ORCID,Sorokin Dimitry Y.910ORCID,Hallsworth John E.11ORCID,Yakimov Michail M.1ORCID

Affiliation:

1. Institute of Polar Research, ISP‐CNR Messina Italy

2. National Council of Research, CNR Rome Italy

3. Department of Biochemistry, Genetics and Microbiology, Faculty of Natural and Agricultural Sciences, Centre for Bioinformatics and Computational Biology University of Pretoria Pretoria South Africa

4. Instituto de Catalisis y Petroleoquimica (ICP), CSIC Madrid Spain

5. Institute for Cellular and Intracellular Symbiosis Ural Branch, Russian Academy of Sciences Orenburg Russia

6. School of Biological Sciences Bangor University Bangor UK

7. Central Facility for Microbiology Helmholtz Centre for Infection Research Braunschweig Germany

8. Institut Pasteur Université Paris Cité, Archaeal Virology Unit Paris France

9. Winogradsky Institute of Microbiology Research Centre of Biotechnology, Russian Academy of Sciences Moscow Russia

10. Department of Biotechnology Delft University of Technology Delft The Netherlands

11. Institute for Global Food Security, School of Biological Sciences Queen's University Belfast Northern Ireland UK

Abstract

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.

Funder

Agence Nationale de la Recherche

European Commission

H2020 Food

Ministerio de Ciencia e Innovación

Publisher

Wiley

Subject

Applied Microbiology and Biotechnology,Biochemistry,Bioengineering,Biotechnology

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