Differential polysaccharide utilization is the basis for a nanohaloarchaeon : haloarchaeon symbiosis

Abstract

Nanohaloarchaeota, a clade of diminutive archaea, with small genomes and limited metabolic capabilities, are ubiquitous in hypersaline habitats, which they share with the extremely halophilic and phylogenetically distant euryarchaea. Some of these nanohaloarchaeota and euryarchaea appear to interact with each other. In this study, we investigate the genetic and physiological nature of their relationship. We isolated the nanohaloarchaeon Candidatus Nanohalobium constans LC1Nh and the haloarchaeon Halomicrobium sp. LC1Hm from a solar saltern, reproducibly co-cultivated these species, sequenced their genomes, and characterized their metabolic/trophic interactions. The nanohaloarchaeon is a magnesium-dependent aerotolerant heterotrophic anaerobe of the DPANN superphylum; it lacks respiratory complexes and its energy production relies on fermentative metabolism of sugar derivatives, obtained by depolymerizing alpha-glucans or by acquiring the chitin monomer N-acetylglucosamine from the chitinolytic haloarchaeal host. Halomicrobium is a member of the class Halobacteria and a chitinotrophic aerobe. The nanohaloarchaeon lacks key biosynthetic pathways and is likely to be provided with amino acids, lipids, nucleotides and cofactors via physical contact with its host Halomicrobium. In turn, the ability of Ca. Nanohalobium to hydrolyse alpha-glucans boosts the host’s growth in the absence of a chitin substrate. These findings suggest that at least some members of the nanohaloarchaea, previously considered ecologically unimportant given their limited metabolic potential, in fact may play significant roles in the microbial carbon turnover, food chains, and ecosystem function. The behaviour of Halomicrobium, which accommodates the colonization by Ca. Nanohalobium, can be interpreted as a bet-hedging strategy, maximizing its long-term fitness in a habitat where the availability of carbon substrates can vary both spatially and temporarily.

Deciphering symbiotic interactions of ‘Candidatus Aenigmarchaeota’ with inferred horizontal gene transfers and co-occurrence networks

“…4c). Other HGT-derived genes could be traced to Euryarchaeota and TACK superphylum archaea, indicating a potential host-symbiont relationship, consistent with previous studies reporting symbioses between DPANN and TACK archaea and Euryarchaeota [10,16,48,49,50].…”

Abundant Taxa and Favorable Pathways in the Microbiome of Soda-Saline Lakes in Inner Mongolia

“…More recently, Ca. Nanahalobium has been proven to be capable of hydrolyzing alpha-glucans (La Cono et al, 2019). Amylase genes were widely distributed in Ca.…”

The evolutionary origins of extreme halophilic Archaeal lineages

“…The red (R) indicators represent the different placements proposed for the Nanohaloarchaea, while the purple (P) indicators are used for the Methanonatronarchaeia. Sources for each placement: R1 (Narasingarao et al, 2012) , R2 (Andrade et al, 2015) , R3 (Aouad et al, 2018); P1 (Sorokin et al, 2017) , and P2 (Aouad et al, 2019). be highly recombinogenic (Mohan et al, 2014;Naor et al, 2012) and are likely physically associated with at least some of the Nanohaloarchaea (Andrade et al, 2015;Cono et al, 2019;Hamm et al, 2019).…”

“…The Haloarchaea are known to be highly recombinogenic (Boucher et al, 2004;Méheust et al, 2018;Mohan et al, 2014;Naor et al, 2012;D. Williams et al,2012) and are physically associated with at least some of the Nanohaloarchaea (Andrade et al, 2015;Cono et al, 2019;Hamm et al, 2019).…”