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

Allbwn ymchwil: Cyfraniad at gyfnodolynErthygladolygiad gan gymheiriaid

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  • Violetta La Cono
    Italian National Research council
  • Enzo Messina
    Italian National Research council
  • Manfred Rohde
    Helmholtz Centre for Infection Research
  • Erika Arcadi
    Italian National Research council
  • Sergio Ciordia
    Institute of Food Science, Technology and Nutrition (ICTAN), Spanish National Research Council (CSIC), Madrid, Spain.
  • Francesca Crisafi
    Italian National Research council
  • Renata Denaro
    Italian National Research council
  • Manuel Ferrer
    Institute of Food Science, Technology and Nutrition (ICTAN), Spanish National Research Council (CSIC), Madrid, Spain.
  • Laura Giuliano
    Mediterranean Science Commission (CIESM)
  • Peter Golyshin
  • Olga Golyshina
  • John E. Hallsworth
    Queen's University, Belfast
  • Gina La Spada
    Italian National Research council
  • Maria C. Mena
    Institute of Food Science, Technology and Nutrition (ICTAN), Spanish National Research Council (CSIC), Madrid, Spain.
  • Alexander Y. Merkel
    Russian Academy of Sciences
  • Margarita A. Shevchenko
    Immanuel Kant Baltic Federal University, Kaliningrad.
  • Francisco Smedile
    Italian National Research council
  • Dimitry Y. Sorokin
    Russian Academy of Sciences
  • Stepan V. Toshchakov
    National Research Center “Kurchatov Institute”, Moscow
  • Michail M. Yakimov
    Italian National Research council
Nano-sized archaeota, with their small genomes and limited metabolic 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, lacking key anabolic machinery and respiratory complexes. The nanohaloarchaeon 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 produce 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 suggests, 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.
Iaith wreiddiolSaesneg
Tudalennau (o-i)20223-20234
Nifer y tudalennau12
CyfnodolynProceedings of the National Academy of Sciences of the USA
Cyfrol117
Rhif y cyfnodolyn33
Dyddiad ar-lein cynnar5 Awst 2020
Dynodwyr Gwrthrych Digidol (DOIs)
StatwsCyhoeddwyd - 18 Awst 2020

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