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Comparative metagenomic analyses of a high-altitude Himalayan geothermal spring revealed temperature-constrained habitat-specific microbial community and metabolic dynamics

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Abstract

Metagenomic surveys across microbial mat (~ 55 °C) samples of high-altitude (1760 m above sea level) Himalayan geothermal springs have revealed specialized community enriched with niche-specific functions. In this study, we have performed metagenomic sequence-based analyses to get insights into taxonomic composition and functional potential of hyperthermophiles in water (~ 95 °C) and sediment samples (78–98 °C). Community analyses revealed predominance of thermophilic bacterial and archeal genera dwelling in water in contrast to microbial mats (55 °C), namely Methylophilus, Methyloversatilis, Emticicia, Caulobacter, Thermus, Enhydrobacter and Pyrobaculum. Sediment samples having surface temperature (~ 78 °C) were colonized by Pyrobaculum and Chloroflexus while genus Massilia was found to be inhabited in high-temperature sediments (~ 98 °C). Functional analyses of metagenomic sequences revealed genetic enrichment of genes such as type IV secretion system, flagellar assembly and two-component system in contrast to mats. Furthermore, inter-sample comparison of enriched microbial diversity among water, sediment and microbial mats revealed habitat-specific clustering of the samples within same environment highlighting the role of temperature dynamics in modulating community structure across different habitats in same niche. However, function-based analysis demonstrated site-specific clustering among sediment, microbial mat and water samples. Furthermore, a novel thermophilic genotype of the genus Emticicia (designated as strain MM) was reconstructed from metagenome data. This is a correlative study between three major habitats present in geothermal spring environment, i.e., water, sediment and microbial mats revealing greater phylogenetic and functional dispersion emphasizing changing habitat-specific dynamics with temperature.

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Acknowledgements

The authors acknowledge funds from Department of Biotechnology (DBT) (BT/PR15118/BCE/8/1141/2015) and Indian Council for Agricultural Research-National Bureau of Agriculturally Important Microorganisms (ICAR-NBAIM). NKM and AS gratefully acknowledge DBT and ICAR-NBAIM for providing research fellowships. This manuscript was revised when RL was on Executive Endeavour Fellowship at Murdoch University, Perth, Australia.

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Correspondence to Rup Lal.

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Communicated by Erko Stackebrandt.

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Mahato, N.K., Sharma, A., Singh, Y. et al. Comparative metagenomic analyses of a high-altitude Himalayan geothermal spring revealed temperature-constrained habitat-specific microbial community and metabolic dynamics. Arch Microbiol 201, 377–388 (2019). https://doi.org/10.1007/s00203-018-01616-6

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