Endemicity of the cosmopolitan mesophilic chemolithoautotroph Sulfurimonas at deep-sea hydrothermal vents

Abstract

Rich animal and microbial communities have been found at deep-sea hydrothermal vents. Although the biogeography of vent macrofauna is well understood, the corresponding knowledge about vent microbial biogeography is lacking. Here, we apply the multilocus sequence analysis (MLSA) to assess the genetic variation of 109 Sulfurimonas strains with ⩾98% 16S rRNA gene sequence similarity, which were isolated from four different geographical regions (Okinawa Trough (OT), Mariana Volcanic Arc and Trough (MVAT), Central Indian Ridge (CIR) and Mid-Atlantic Ridge (MAR)). Sequence typing based on 11 protein-coding genes revealed high genetic variation, including some allele types that are widespread within regions, resulting in 102 nucleotide sequence types (STs). This genetic variation was predominantly due to mutation rather than recombination. Phylogenetic analysis of the 11 concatenated genes showed a clear geographical isolation corresponding to the hydrothermal regions they originated from, suggesting limited dispersal. Genetic differentiation among Sulfurimonas populations was primarily influenced by geographical distance rather than gas composition of vent fluid or habitat, although in situ environmental conditions of each microhabitat could not be examined. Nevertheless, Sulfurimonas may possess a higher dispersal capability compared with deep-sea hydrothermal vent thermophiles. This is the first report on MLSA of deep-sea hydrothermal vent Epsilonproteobacteria, which is indicative of allopatric speciation.

Thermosipho spp. immune system differences affect variation in genome size and geographical distributions

“…Altogether, these results are consistent with the 16S rRNA findings and suggest that isolation by distance is important for Thermosipho spp. differentiation, as observed for other thermophiles ( Mino et al. 2017 ).…”

Deepest and hottest hydrothermal activity in the Okinawa Trough: the Yokosuka site at Yaeyama Knoll

“…All of these Epsilonproteobacteria are mesophilic chemoautotrophs [ 87 ]; however, Thioreductor species lack the ability to use sulfur compounds as the energy source and instead uses H 2 as the primary energy source [ 80 ]. In previous studies in the OT hydrothermal fields, members of Thioreductor had a relatively limited distribution compared with those of Sulfurovum and Sulfurimonas [ 35 , 81 , 84 , 85 ]. For example, in the Iheya North Original hydrothermal site (water depth = approximately 1000 m; maximum fluid temperature = 311°C), members of Campylobacterales were frequently detected in the vicinity of deep-sea hydrothermal vents.…”

“…The narrow range of depths also allows prosperity of similar species which have physiological advantage against the pressure range around 10–15 MPa. In fact, research of microbes and vent fauna inhabiting OT hydrothermal sites in the past decades [ 33 – 35 ] have revealed a well-mixed genetic pool among the OT sites, except the two sites shallower than 900 m [ 36 ]. If a hydrothermal vent site is discovered at another distinct water depth range within the OT, it would provide insights to understand and evaluate the significance of depth, temperature, pressure and fluid chemistry in determining the biodiversity and biogeography.…”

Patterns of (trace) metals and microorganisms in the Rainbow hydrothermal vent plume at the Mid-Atlantic Ridge

“…Despite dilution, the vent-associated group Epsilonproteobacteria (specifically the most common genus Sulfurimonas), appeared to dominate the community composition. This is likely due to its flexibility to exploit a range of electron donors and acceptors (Nakagawa et al, 2005), making them suitable inhabitants of dynamic environments (Huber et al, 2003). From the relative abundance data presented here it cannot be determined whether Epsilonproteobacteria dominate by rapid reproduction or if other groups decline in abundance.…”