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 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.

Physical connections: prokaryotes parasitizing their kin

“…LC1Hm (Fig. 2) seems to be mutualistic, at least under some conditions, and based on different polysaccharide‐metabolizing activities (La Cono et al ., 2020). The haloarchaeon usually degrades chitin extracellularly, producing beta‐glucans that it consumes.…”

“…Nanohalobium ferments glycogen or starch (alpha‐glucans that the host does not metabolize), making their products accessible to the host which, in turn, sustains its metabolically limited epibiont. Nonetheless, whether this strategy maximizes the long‐term fitness of the host (La Cono et al ., 2020) or whether Ca . Nanohalobium becomes parasitic in the presence of chitin and/or in the absence of glycogen or starch in the environment remains to be established.…”

“…B. SEM picture of Candidatus Nanohalobium constans LC1Nh associated to its chitinolytic haloarchaeal host Halomicrobium sp. LC1Hm (La Cono et al ., 2020) (courtesy of M. M. Yakimov). C. Transmission electron microscopy (TEM) image of Nanoarchaeum equitans associated to its hyperthermophilic archaeal host Ignicoccus hospitalis (Huber et al ., 2002) (courtesy of K.O.…”

Metagenome-derived virus-microbe ratios across ecosystems

“…Some of them, notably CPR bacteria, are parasites/predators 26,27 ; others can display mutualistic interactions (e.g. complementation of host’s metabolism to degrade specific substrates 28 ) although, upon environmental change, they likely behave as parasites, shifting along the mutualism-parasitism continuum 29 . Testing these hypotheses ultimately requires reliable quantification of virus-to-cell and episymbiont versus free-living cell ratios that can be comparatively applied across biomes.…”

Metagenomic Insights Into Ecological and Phylogenetic Significances of Candidatus Natranaeroarchaeales, a Novel Abundant Archaeal Order in Soda Lake Sediment

“…Very recently, culture-dependent and -independent researches revealed that Ca. Nanohaloarchaeota had the capability of poly-or oligo-saccharide degradation in hypersaline brines of saltern and soda lakes [12,21]. Besides, the methylotrophic methanogenesis was evidently a dominant process, and many haloalkaliphilic methylotrophic methanogens were isolated from soda lakes, including Methanolobus, Methanosalsum, Methanocalculus and Methanonatronarchaeum [22,23].…”