Comparative genomics reveals adaptations of a halotolerant thaumarchaeon in the interfaces of brine pools in the Red Sea
Ba Alawi, Wail
Hikmawan, Tyas I.
El-Dorry, Hamza A A
Bajic, Vladimir B.
KAUST DepartmentRed Sea Research Center (RSRC)
Computational Bioscience Research Center (CBRC)
Computer, Electrical and Mathematical Sciences and Engineering (CEMSE) Division
Applied Mathematics and Computational Science Program
Biological and Environmental Sciences and Engineering (BESE) Division
Marine Science Program
Marine Microbial Ecology Research Group
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AbstractThe bottom of the Red Sea harbors over 25 deep hypersaline anoxic basins that are geochemically distinct and characterized by vertical gradients of extreme physicochemical conditions. Because of strong changes in density, particulate and microbial debris get entrapped in the brine-seawater interface (BSI), resulting in increased dissolved organic carbon, reduced dissolved oxygen toward the brines and enhanced microbial activities in the BSI. These features coupled with the deep-sea prevalence of ammonia-oxidizing archaea (AOA) in the global ocean make the BSI a suitable environment for studying the osmotic adaptations and ecology of these important players in the marine nitrogen cycle. Using phylogenomic-based approaches, we show that the local archaeal community of five different BSI habitats (with up to 18.2% salinity) is composed mostly of a single, highly abundant Nitrosopumilus-like phylotype that is phylogenetically distinct from the bathypelagic thaumarchaea; ammonia-oxidizing bacteria were absent. The composite genome of this novel Nitrosopumilus-like subpopulation (RSA3) co-assembled from multiple single-cell amplified genomes (SAGs) from one such BSI habitat further revealed that it shares ∼54% of its predicted genomic inventory with sequenced Nitrosopumilus species. RSA3 also carries several, albeit variable gene sets that further illuminate the phylogenetic diversity and metabolic plasticity of this genus. Specifically, it encodes for a putative proline-glutamate 'switch' with a potential role in osmotolerance and indirect impact on carbon and energy flows. Metagenomic fragment recruitment analyses against the composite RSA3 genome, Nitrosopumilus maritimus, and SAGs of mesopelagic thaumarchaea also reiterate the divergence of the BSI genotypes from other AOA.
SponsorsWe are grateful for financial support from the Saudi Aramco (Bio-CCC RGC/3/1051-01) and the SEDCO Research Excellence Award program. We also thank the 3rd WHOI-KAUST Red Sea 2011 Cruise team, the captain and the crew on board the RV Aegeo, and the Coastal and Marine Resources Core Lab (CMRC) for their excellent technical assistance; the Genomics Core Lab Facility for sequencing efforts; and Dr Till Bayer for helpful bio-informatics discussions.
JournalThe ISME Journal
PubMed Central IDPMC4303633
CollectionsArticles; Red Sea Research Center (RSRC); Marine Science Program; Applied Mathematics and Computational Science Program; Computational Bioscience Research Center (CBRC); Biological and Environmental Sciences and Engineering (BESE) Division; Computer, Electrical and Mathematical Sciences and Engineering (CEMSE) Division; Plankton Genomics, part of the Global Ocean Genome Project
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