Distinctive Microbial Community Structure in Highly Stratified Deep-Sea Brine Water Columns

Abstract

b Atlantis II and Discovery are two hydrothermal and hypersaline deep-sea pools in the Red Sea rift that are characterized by strong thermohalo-stratification and temperatures steadily peaking near the bottom. We conducted comprehensive vertical profiling of the microbial populations in both pools and highlighted the influential environmental factors. Pyrosequencing of the 16S rRNA genes revealed shifts in community structures vis-à-vis depth. High diversity and low abundance were features of the deepest convective layers despite the low cell density. Surprisingly, the brine interfaces had significantly higher cell counts than the overlying deep-sea water, yet they were lowest in diversity. Vertical stratification of the bacterial populations was apparent as we moved from the Alphaproteobacteria-dominated deep sea to the Planctomycetaceae-or Deferribacteres-dominated interfaces to the Gammaproteobacteria-dominated brine layers. Archaeal marine group I was dominant in the deep-sea water and interfaces, while several euryarchaeotic groups increased in the brine. Across sites, microbial phylotypes and abundances varied substantially in the brine interface of Discovery compared with Atlantis II, despite the near-identical populations in the overlying deep-sea waters. The lowest convective layers harbored interestingly similar microbial communities, even though temperature and heavy metal concentrations were very different. Multivariate analysis indicated that temperature and salinity were the major influences shaping the communities. The harsh conditions and the low-abundance phylotypes could explain the observed correlation in the brine pools. The Red Sea, a part of the Great Rift Valley, was formed when the Arabian plate split from the African plate. Due to the high surface temperature, excess evaporation, and scarcity of rainfall coupled with a lack of a major source of fresh water influx, the Red Sea is one of the hottest and saltiest seawater bodies in the world. Over the past 40 years, oceanographers have discovered 25 brinefilled deeps in the rift valley of the Red Sea (1-6). These deeps are characterized by their anoxic, hypersaline, hyperthermal, and metalliferous conditions at the bottom, representing some of the most unusual and extreme environments on earth (4, 7-9).The deep-sea brine pools Atlantis II and Discovery, which are located in the middle axial rift zone of the Red Sea, represent a rare type of extreme environment with both hypersaline and hydrothermal geochemical characteristics. Since their discovery in 1965, detailed geological and geochemical investigations have been carried out on these two deeps (1). The Atlantis II Deep is a hydrothermally active brine pool with a temperature that has continuously increased from the earliest record of 44.8°C (1, 10) to the current recorded temperature of 68°C. This increase has been attributed to the influx of hot brine supplied by a geyser spring at the bottom of the Atlantis II pool (11), which divides the brine into two stratified anoxic layers with s...

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

“…In contrast, dissolved oxygen is present at relatively low concentrations in the BSI compared with the deep-seawater mass in the Red Sea (B1-5 mM vs B90 mM; Ngugi and Stingl, 2012; The total iron content in the BSI (B0.01-70 mM) is much higher than in the deep-seawater (o0.1 mM; Danielsson et al, 1980), whereas manganese is very high (up to 1.7 mM) and seems to rise with increasing salinity of the brine. Owing to their high concentration (Table 1), affinity and possible precipitation with other elements (Krom and Berner, 1980), these two ions may exacerbate the already limited availability of some essential nutrients in the BSI, for example, phosphate (o1 mM; Karbe, 1987;Bougouffa et al, 2013). Sulfate concentrations broadly decreased from normal-seawater levels (B30 mM) to about 10 mM in the brine, indicating sulfate reduction in the anoxic brine layers.…”

“…Here also, the concentration of nutrients (organic carbon, NH 4 þ and NO 3 -) and minerals are a few orders of magnitude higher than in the overlying seawater (Ryan et al, 1969;Anschutz et al, 1999;Bougouffa et al, 2013).…”

“…For example, RSA3 and SCM1 are the only members of their genus harboring a putative high-affinity phosphate-specific transport (Pst) system (pstSCABU; Nmar_0479/ 0481-0484; Figure 3b), which might be correlated with the extremely low concentration of dissolved inorganic phosphate in the Atlantis-BSI (o1 mM; Bougouffa et al, 2013); the other species are predicted to have the low-affinity phosphate inorganic transporter. The Pst system occurs also in non-marine thaumarchaea (Kim et al, 2011;Blainey et al, 2011;Spang et al, 2012; Figure 3b), suggesting that phosphorus limitation is not necessarily confined to marine Thaumarchaeota.…”

“…Molecular-based evidences and geochemical data gathered in all brine pools studied to date document that sulfur cycling and aerobic oxidation of methane are the main energy-generating processes in the BSI habitat (Faber et al, 1998;Eder et al, 2002;Schmidt et al, 2003;Daffonchio et al, 2006;Yakimov et al, 2007;Borin et al, 2009;Joye et al, 2009;La Cono et al, 2011;Ferrer et al, 2012;Bougouffa et al, 2013). Although ammonia-oxidizing archaea (AOA) typically predominate the deep-sea realm of the global ocean (Stahl and de la Torre, 2012; and references therein), data from some Mediterranean Sea brines suggest that Archaea are less predominant in the BSI environment (B10% of all prokaryotes; Daffonchio et al, 2006;Yakimov et al, 2007;Borin et al, 2009).…”

“…Moreover, the BSI is a microbial 'hotspot' harboring dense microbial populations, which are also metabolically more active than the adjacent layers (Karbe, 1987;Daffonchio et al, 2006;Yakimov et al, 2007;Bougouffa et al, 2013).…”