Nanohaloarchaea as beneficiaries of xylan degradation by haloarchaea
Creators
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La Cono, Violetta1
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Messina, Enzo2
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Reva, Olga3
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Smedile, Francesco1
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La Spada, Gina1
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Crisafi, Francesca1
- Marturano, Laura1
- Miguez, Noa4
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Ferrer, Manuel4
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Selivanova, Elena A5
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Golyshina, Olga V6
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Golyshin, Peter N6
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Rohde, Manfred7
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Krupovic, Mart8
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Merkel, Alexander Y9
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Sorokin, Dimitry Y10
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Hallsworth, John E11
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Yakimov, Michail M1
- 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. Winogradsky Institute of Microbiology, Research Centre of Biotechnology, Russian Academy of Sciences, Moscow, Russia; 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
Description
Climate 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.
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Additional details
Funding
- INMARE – Industrial Applications of Marine Enzymes: Innovative screening and expression platforms to discover and use the functional protein diversity from the sea 634486
- European Commission
- FuturEnzyme – Technologies of the Future for Low-Cost Enzymes for Environment-Friendly Products 101000327
- European Commission
- VIROMET – Uncovering the virome of archaeal methanogens ANR-20-CE20-0009
- Agence Nationale de la Recherche