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Nanohaloarchaea as beneficiaries of xylan degradation by haloarchaea

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 plan...

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Autores principales: La Cono, Violetta, Messina, Enzo, Reva, Oleg, Smedile, Francesco, La Spada, Gina, Crisafi, Francesca, Marturano, Laura, Miguez, Noa, Ferrer, Manuel, Selivanova, Elena A., Golyshina, Olga V., Golyshin, Peter N., Rohde, Manfred, Krupovic, Mart, Merkel, Alexander Y., Sorokin, Dimitry Y., Hallsworth, John E., Yakimov, Michail M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10443357/
https://www.ncbi.nlm.nih.gov/pubmed/37317055
http://dx.doi.org/10.1111/1751-7915.14272
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author La Cono, Violetta
Messina, Enzo
Reva, Oleg
Smedile, Francesco
La Spada, Gina
Crisafi, Francesca
Marturano, Laura
Miguez, Noa
Ferrer, Manuel
Selivanova, Elena A.
Golyshina, Olga V.
Golyshin, Peter N.
Rohde, Manfred
Krupovic, Mart
Merkel, Alexander Y.
Sorokin, Dimitry Y.
Hallsworth, John E.
Yakimov, Michail M.
author_facet La Cono, Violetta
Messina, Enzo
Reva, Oleg
Smedile, Francesco
La Spada, Gina
Crisafi, Francesca
Marturano, Laura
Miguez, Noa
Ferrer, Manuel
Selivanova, Elena A.
Golyshina, Olga V.
Golyshin, Peter N.
Rohde, Manfred
Krupovic, Mart
Merkel, Alexander Y.
Sorokin, Dimitry Y.
Hallsworth, John E.
Yakimov, Michail M.
author_sort La Cono, Violetta
collection PubMed
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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spelling pubmed-104433572023-08-23 Nanohaloarchaea as beneficiaries of xylan degradation by haloarchaea La Cono, Violetta Messina, Enzo Reva, Oleg Smedile, Francesco La Spada, Gina Crisafi, Francesca Marturano, Laura Miguez, Noa Ferrer, Manuel Selivanova, Elena A. Golyshina, Olga V. Golyshin, Peter N. Rohde, Manfred Krupovic, Mart Merkel, Alexander Y. Sorokin, Dimitry Y. Hallsworth, John E. Yakimov, Michail M. Microb Biotechnol Research Articles 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. John Wiley and Sons Inc. 2023-06-14 /pmc/articles/PMC10443357/ /pubmed/37317055 http://dx.doi.org/10.1111/1751-7915.14272 Text en © 2023 The Authors. Microbial Biotechnology published by Applied Microbiology International and John Wiley & Sons Ltd. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle Research Articles
La Cono, Violetta
Messina, Enzo
Reva, Oleg
Smedile, Francesco
La Spada, Gina
Crisafi, Francesca
Marturano, Laura
Miguez, Noa
Ferrer, Manuel
Selivanova, Elena A.
Golyshina, Olga V.
Golyshin, Peter N.
Rohde, Manfred
Krupovic, Mart
Merkel, Alexander Y.
Sorokin, Dimitry Y.
Hallsworth, John E.
Yakimov, Michail M.
Nanohaloarchaea as beneficiaries of xylan degradation by haloarchaea
title Nanohaloarchaea as beneficiaries of xylan degradation by haloarchaea
title_full Nanohaloarchaea as beneficiaries of xylan degradation by haloarchaea
title_fullStr Nanohaloarchaea as beneficiaries of xylan degradation by haloarchaea
title_full_unstemmed Nanohaloarchaea as beneficiaries of xylan degradation by haloarchaea
title_short Nanohaloarchaea as beneficiaries of xylan degradation by haloarchaea
title_sort nanohaloarchaea as beneficiaries of xylan degradation by haloarchaea
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10443357/
https://www.ncbi.nlm.nih.gov/pubmed/37317055
http://dx.doi.org/10.1111/1751-7915.14272
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