| Title | Symbiosis between nanohaloarchaeon and haloarchaeon is based on utilization of different polysaccharides |
| Abstract | 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 betaglucan 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. |
| Source | Proceedings of the National Academy of Sciences of the United States of America 117 (33), pp. 20223–20234 |
| Keywords | HaloarchaeaNanohaloarchaeaPolysaccharide utilizationSolar salternsSymbiosis |
| Journal | Proceedings of the National Academy of Sciences of the United States of America |
| Editor | The Academy,, Washington, D.C., Stati Uniti d'America |
| Year | 2020 |
| Type | Articolo in rivista |
| DOI | 10.1073/PNAS.2007232117 |
| Authors | La Cono, Violetta; Messina, Enzo; Rohde, Manfred; Arcadi, Erika; Ciordia, Sergio; Crisafi, Francesca; Denaro, Renata; Ferrer, Manuel; Giuliano, Laura; Golyshin, Peter N.; Golyshina, Olga V.; Hallsworth, John E.; la Spada, Gina; Mena, Maria C.; Merkel, Alexander Y.; Shevchenko, Margarita A.; Smedile, Francesco; Sorokin, Dimitry Y.; Toshchakov, Stepan V.; Yakimov, Michail M. |
| Text | 445724 2020 10.1073/PNAS.2007232117 Scopus 2 s2.0 85089786784 Haloarchaea Nanohaloarchaea Polysaccharide utilization Solar salterns Symbiosis Symbiosis between nanohaloarchaeon and haloarchaeon is based on utilization of different polysaccharides La Cono, Violetta; Messina, Enzo; Rohde, Manfred; Arcadi, Erika; Ciordia, Sergio; Crisafi, Francesca; Denaro, Renata; Ferrer, Manuel; Giuliano, Laura; Golyshin, Peter N.; Golyshina, Olga V.; Hallsworth, John E.; la Spada, Gina; Mena, Maria C.; Merkel, Alexander Y.; Shevchenko, Margarita A.; Smedile, Francesco; Sorokin, Dimitry Y.; Toshchakov, Stepan V.; Yakimov, Michail M. Winogradsky Institute of Microbiology, Russian Academy of Sciences; Immanuel Kant Baltic Federal University; Queen s University Belfast; Bangor University; CSIC Instituto de Cat amp;aacute;lisis y Petroleoqu amp;iacute;mica ICP ; Consiglio Nazionale delle Ricerche; National Research Centre Kurchatov Institute ; CSIC Centro Nacional de Biotecnologia CNB ; Helmholtz Centre for Infection Research HZI ; Delft University of Technology; Mediterranean Science Commission CIESM 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 betaglucan 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. 117 Published version http //www.scopus.com/record/display.url eid=2 s2.0 85089786784 origin=inward LaCono et al., 2020 article 20223.full.pdf Articolo in rivista The Academy, 0027 8424 Proceedings of the National Academy of Sciences of the United States of America Proceedings of the National Academy of Sciences of the United States of America Proc. Natl. Acad. Sci. U.S.A. Proceedings of the National Academy of Sciences of the United States of America. PNAS mikhail.iakimov IAKIMOV MIKHAIL renata.denaro DENARO RENATA violetta.lacono LA CONO VIOLETTA enzo.messina MESSINA ENZO francesco.smedile SMEDILE FRANCESCO francesca.crisafi CRISAFI FRANCESCA INMARE Industrial Applications of Marine Enzymes Innovative screening and expression platforms to discover and use the functional protein diversity from the sea |
