4.8 Article

Symbiosis between nanohaloarchaeon and haloarchaeon is based on utilization of different polysaccharides

Publisher

NATL ACAD SCIENCES
DOI: 10.1073/pnas.2007232117

Keywords

haloarchaea; nanohaloarchaea; polysaccharide utilization; symbiosis; solar salterns

Funding

  1. Italian Ministry of University and Research under the RITMARE Flagship Project (2012-2016)
  2. Italian Ministry of University and Research under the INMARE Project - European Union's Horizon 2020 Research Program [H2020-BG-2014-2634486]
  3. Centre for Environmental Biotechnology Project - European Regional Development Fund via the Welsh Assembly Government
  4. SYAM-Gravitation Program of the Dutch Ministry of Education and Science Grant [24002002]
  5. Russian Foundation for Basic Research Grant [19-04-00401]
  6. Ministry of Science and Higher Education of Russian Federation [075-15-2019-1659]

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Nano-sized archaeota, with their small genomes and limited meta-bolic capabilities, are known to associate with other microbes, thereby compensating for their own auxotrophies. These diminutive and yet ubiquitous organisms thrive in hypersaline habitats that they share with haloarchaea. Here, we reveal the genetic and physiological nature of a nanohaloarchaeon-haloarchaeon association, with both microbes obtained from a solar saltern and reproducibly cultivated together in vitro. The nanohaloarchaeon Candidatus Nanohalobium constans LC1Nh is an aerotolerant, sugar-fermenting anaerobe, lack-ing key anabolic machinery and respiratory complexes. The nanoha-loarchaeon cells are found physically connected to the chitinolytic haloarchaeon Halomicrobium sp. LC1Hm. Our experiments revealed that this haloarchaeon can hydrolyze chitin outside the cell (to pro-duce the monosaccharide N-acetylglucosamine), using this beta-glucan to obtain carbon and energy for growth. However, LC1Hm could not metabolize either glycogen or starch (both alpha-glucans) or other polysaccharides tested. Remarkably, the nanohaloarchaeon's ability to hydrolyze glycogen and starch to glucose enabled growth of Halomicrobium sp. LC1Hm in the absence of a chitin. These findings indicated that the nanohaloarchaeon-haloarchaeon association is both mutualistic and symbiotic; in this case, each microbe relies on its partner's ability to degrade different polysaccharides. This sug-gests, in turn, that other nano-sized archaeota may also be beneficial for their hosts. Given that availability of carbon substrates can vary both spatially and temporarily, the susceptibility of Halomicrobium to colonization by Ca. Nanohalobium can be interpreted as a strategy to maximize the long-term fitness of the host.

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