Comparative genomics reveals adaptations of a halotolerant thaumarchaeon in the interfaces of brine pools in the Red Sea

Abstract

The 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 B54% 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.

Genomic and Transcriptomic Evidence for Carbohydrate Consumption among Microorganisms in a Cold Seep Brine Pool

“…But for novel phyla without many available genomes in public databases, comparing to single-cell amplified genomes (SAGs) from similar habitats is a more effective approach. The Thaumarchaeota genome binned in the present study possesses a gene inventory that is nearly identical to the SAGs from another Red Sea brine pool (Ngugi et al, 2015); this is strong evidence that the genome binning approach employed here is highly accurate.…”

“…nov. 1 (TCS50) and 91.3% of the Thaumarchaeota sp. nov. 2 (TCS51) could be assigned to the eight single-cell Thaumarchaeota genomes, which were from another brine pool in the Red Sea (Ngugi et al, 2015). The assigned ORFs were distributed in all of the contigs of the TCS MAGs as exemplified by Thaumarchaeota sp.…”

“…Moreover, the Thaumarchaeota MAGs in the present study were compared with the eight genomes obtained using single-cell genomics by Ngugi et al (2015), based on BLASTP (e-value < 1e-07) and BLASTN (e-value < 1e-07) with predicted open reading frames (ORFs) as input. The results were visualized using the Artemis Comparison Tool (ACT; Carver et al, 2005).…”

“…Studies of microbial lifestyles in brine pools are less common than those of hydrothermal vents. The brine pools studied so far include the Shaban Deep (Ferrer et al, 2012), Discovery Deep (Wang et al, 2013), Atlantis II Deep (Ngugi et al, 2015), and Kebrit Deep (Guan et al, 2015) of the Red Sea, which contains more than 25 deep hypersaline anoxic pools (Antunes et al, 2011). Previous investigations of other deep-sea brine pools included those in the Mediterranean Sea (van der Wielen et al, 2005) and the Gulf of Mexico (Formolo and Lyons, 2013).…”

“…As a consequence, the prevalent processes in the microbial inhabitants are anaerobic oxidation of methane and sulfite and sulfate reduction (Antunes et al, 2011). Surveys of brine pools identified a few widespread groups including Proteobacteria, Actinobacteria, Cyanobacteria, and Deferribacteres, and showed a higher diversity of bacteria over the archaea (Ferrer et al, 2012; Guan et al, 2015; Ngugi et al, 2015). Despite the common origin and shared features of the investigated brine pools, regional variation may lead to distinct combinations of physicochemical parameters and sustains microorganisms with unique adaptive strategies.…”