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Highly integrated adaptive mechanisms in Spiribacter halalkaliphilus, a bacterium abundant in Chinese soda-saline lakes.

ABSTRACT: Soda-saline lakes are polyextreme environments inhabited by many haloalkaliphiles, including one of the most abundant Spiribacter species. However, its mechanisms of adaptation are not ecophysiologically characterized. Based on a large-scale cultivation strategy, we obtained a representative isolate of this Spiribacter species whose relative abundance was the highest (up to 15.63%) in a wide range of salinities in the soda-saline lakes in Inner Mongolia, China. This species is a chemoorganoheterotrophic haloalkaliphile. It has a small and streamlined genome and utilizes a wide variety of compatible solutes to resist osmotic pressure and multiple monovalent cation/proton antiporters for pH homeostasis. In addition to growth enhancement by light under microaerobic conditions, cell growth, organic substrate consumption and polyhydroxybutyrate biosynthesis were also improved by inorganic sulfide. Both quantitative RT-PCR and enzymatic assays verified that sulfide:quinone oxidoreductase was upregulated during this process. Metatranscriptomic analysis indicated that all genes related to environmental adaptation were transcribed in natural environments. Overall, this study has identified a novel abundant haloalkaliphile with multiple and highly integrated adaptive strategies and found that inorganic sulfide was able to improve the adaptation of a heterotroph to polyextreme environments.

SUBMITTER: Xue Q

PROVIDER: S-EPMC9292931 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Soda-saline lakes are a special type of alkaline lake in which the chloride concentration is greater than the carbonate/bicarbonate concentration. Due to the high pH and a usually higher osmotic pressure than that of a normal soda lake, the microbes may need more energy to thrive in such a double-extreme environment. In this study, we systematically investigated the microbiome of the brine and sediment samples of nine artificially separated ponds (salinities from 5.5% to saturation) within two soda-saline lakes in Inner Mongolia of China, assisted by deep metagenomic sequencing. The main inorganic ions shaped the microbial community in both the brines and sediments, and the chloride concentration exhibited the most significant effect. A total of 385 metagenome-assembled genomes (MAGs) were generated, in which 38 MAGs were revealed as the abundant species in at least one of the eighteen different samples. Interestingly, these abundant species also represented the most branches of the microbiome of the soda-saline lakes at the phylum level. These abundant taxa were close relatives of microorganisms from classic soda lakes and neutral saline environments, but forming a combination of both habitats. Notably, approximately half of the abundant MAGs had the potential to drive dissimilatory sulfur cycling. These MAGs included four autotrophic Ectothiorhodospiraceae MAGs, one Cyanobacteria MAG and nine heterotrophic MAGs with the potential to oxidize sulfur, as well as four abundant MAGs containing genes for elemental sulfur respiration. The possible reason is that reductive sulfur compounds could provide additional energy for the related species, and reductions of oxidative sulfur compounds are more prone to occur under alkaline conditions which support the sulfur cycling. In addition, a unique 1,4-alpha-glucan phosphorylation pathway, but not a normal hydrolysis one, was found in the abundant Candidatus Nanohaloarchaeota MAG NHA-1, which would produce more energy in polysaccharide degradation. In summary, this work has revealed the abundant taxa and favorable pathways in the soda-saline lakes, indicating that efficient energy regeneration pathway may increase the capacity for environmental adaptation in such saline-alkaline environments. These findings may help to elucidate the relationship between microbial metabolism and adaptation to extreme environments.

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Highly integrated adaptive mechanisms in Spiribacter halalkaliphilus, a bacterium abundant in Chinese soda-saline lakes.

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