Nanohaloarchaea as beneficiaries of xylan degradation by haloarchaea

Abstract

Climate change, desertification, salinisation of soils and the changing hydrology of the Earth are creating or modifying microbial habitats at all scales including the oceans, saline groundwaters and brine lakes. In environments that are saline or hypersaline, the biodegradation of recalcitrant plant and animal polysaccharides can be inhibited by salt‐induced microbial stress and/or by limitation of the metabolic capabilities of halophilic microbes. We recently demonstrated that the chitinolytic haloarchaeon Halomicrobium can serve as the host for an ectosymbiont, nanohaloarchaeon ‘Candidatus Nanohalobium constans’. Here, we consider whether nanohaloarchaea can benefit from the haloarchaea‐mediated degradation of xylan, a major hemicellulose component of wood. Using samples of natural evaporitic brines and anthropogenic solar salterns, we describe genome‐inferred trophic relations in two extremely halophilic xylan‐degrading three‐member consortia. We succeeded in genome assembly and closure for all members of both xylan‐degrading cultures and elucidated the respective food chains within these consortia. We provide evidence that ectosymbiontic nanohaloarchaea is an active ecophysiological component of extremely halophilic xylan‐degrading communities (although by proxy) in hypersaline environments. In each consortium, nanohaloarchaea occur as ectosymbionts of Haloferax, which in turn act as scavenger of oligosaccharides produced by xylan‐hydrolysing Halorhabdus. We further obtained and characterised the nanohaloarchaea–host associations using microscopy, multi‐omics and cultivation approaches. The current study also doubled culturable nanohaloarchaeal symbionts and demonstrated that these enigmatic nano‐sized archaea can be readily isolated in binary co‐cultures using an appropriate enrichment strategy. We discuss the implications of xylan degradation by halophiles in biotechnology and for the United Nation's Sustainable Development Goals.

Functional diversity of nanohaloarchaea within xylan-degrading consortia

“…Rather than being the instrument responsible for intracellular invasion into the host (Hamm et al, 2023 ), these proteins likely function as secretion channels (straws) through which the nanohaloarchaeon can inject effector(s) that favorably affect the host metabolism. The latter possibility is supported by our recent results demonstrating a 50-fold increase in the production of glucose-6-phosphate in Haloferax lucentense cells associated with the SVXNc symbiont compared with axenic culture of the host (La Cono et al, 2023 ).…”

“…High overall collinearity and high similarity in terms of the gene context (>70% of amino acid identity) were found between all of them along with the presence of a few organism-specific genome rearrangements, such as the giant proteins and several genomic islands ( Figure 1 ). These findings strongly suggest the common origin of all these nanohaloarchaea, even though they were isolated from geographically distinct sites and have different haloarchaeal hosts (La Cono et al, 2020 , 2023 ).…”

“…In the absence of any of the respiratory complexes, both strains of nanohaloarchaea must stick to a strictly anaerobic fermentative lifestyle. However, they are obligatory-dependent on their aerobic host Haloferax lucertense (La Cono et al, 2023 ). Inhabiting aerobic environments requires an extended tolerance to oxidative stress.…”

“…The only exception is the uncultivated nanohaloarchaeon M3_22 (Feng et al, 2021 ), which likely belongs to the same genus Ca . Nanohalovita (La Cono et al, 2023 ). In analogy to what is known as haloarchaeal PST (Eichler and Maupin-Furlow, 2013 ), the PTS of Ca .…”

“…Nanohalovita haloferacivicina. Our recent study to stably cultivate these nanohaloarchaea as members of xylan-degrading haloarchaeal consortia, obtained from brines and sediments of two distant hypersaline ecosystems (La Cono et al, 2023 ), has enabled the current study of their functional diversity that is key to understanding their ecology in nature. Metabolism, functional prediction of unique features, and both interaction with hosts and defense mechanisms were inferred from their cultivation experiments in binary cultures, whole genomes, transcriptomics, and DNA methylome analyses.…”