Co-registered Geochemistry and Metatranscriptomics Reveal Unexpected Distributions of Microbial Activity within a Hydrothermal Vent Field

Abstract

Despite years of research into microbial activity at diffuse flow hydrothermal vents, the extent of microbial niche diversity in these settings is not known. To better understand the relationship between microbial activity and the associated physical and geochemical conditions, we obtained co-registered metatranscriptomic and geochemical data from a variety of different fluid regimes within the ASHES vent field on the Juan de Fuca Ridge. Microbial activity in the majority of the cool and warm fluids sampled was dominated by a population of Gammaproteobacteria (likely sulfur oxidizers) that appear to thrive in a variety of chemically distinct fluids. Only the warmest, most hydrothermally-influenced flows were dominated by active populations of canonically vent-endemic Epsilonproteobacteria. These data suggest that the Gammaproteobacteria collected during this study may be generalists, capable of thriving over a broader range of geochemical conditions than the Epsilonproteobacteria. Notably, the apparent metabolic activity of the Gammaproteobacteria—particularly carbon fixation—in the seawater found between discrete fluid flows (the intra-field water) suggests that this area within the Axial caldera is a highly productive, and previously overlooked, habitat. By extension, our findings suggest that analogous, diffuse flow fields may be similarly productive and thus constitute a very important and underappreciated aspect of deep-sea biogeochemical cycling that is occurring at the global scale.

Spatially distinct, temporally stable microbial populations mediate biogeochemical cycling at and below the seafloor in hydrothermal vent fluids

“…Mesophilic and psychrophilic Gammaproteobacteria, namely SUP05, as well as Epsilonbacteraeota were the dominant organisms present and genes for metabolisms like sulfur oxidation, which can be carried out under aerobic and microaerobic conditions, were most abundant at Anemone (Figs and ). These results are supported by a study of diffuse vent sites within the ASHES vent field, which showed similar community composition and gene expression patterns as those observed at Anemone (Olins et al ., ). The genomic binning results also support this model, as SUP05 populations had higher gene expression levels at Anemone compared to other diffuse vents.…”

“…() showed that there were fine‐scale phylogenetic differences in microbial community structure between the two vent fields, with fluid communities at each vent field more closely related to one another than communities found in fluids from the other vent field. In addition, smaller scale spatial studies of multiple diffuse vents within one vent field (Huber et al ., ; Opatkiewicz et al ., ; Perner et al ., ; Akerman et al ., ; Meier et al ., ; Olins et al ., ) show that the microbial community composition is shaped by both the geochemistry as well as the distance between individual diffuse vents. For example, Akerman et al .…”

“…At active hydrothermal systems, cold, oxidized seawater mixes with hot, chemically reduced hydrothermal fluids at and below the seafloor, forming low-temperature diffuse vent fluids that contain abundant energy sources to support taxonomically and metabolically diverse microbial communities (Jannasch and Mottl, 1985;Karl, 1995;Reysenbach and Shock, 2002;Huber et al, 2007;Perner et al, 2009;Amend et al, 2011;Olins et al, 2017). Examination of these mixed diffuse fluids allows for inferences about microbially mediated processes occurring beneath the seafloor, where various subseafloor habitats are predicted to exist spanning oxic to anoxic conditions and temperatures of 58C to greater than 1008C (Huber et al, 2002;Butterfield et al, 2004;Sievert and Vetriani, 2012;Fortunato and Huber, 2016).…”

“…In a regional-scale study comparing the communities in diffuse fluids from two vent fields with distinct geology and chemistry located within 20 km of one another on the Mid-Cayman Rise, Reveillaud et al (2016) showed that there were fine-scale phylogenetic differences in microbial community structure between the two vent fields, with fluid communities at each vent field more closely related to one another than communities found in fluids from the other vent field. In addition, smaller scale spatial studies of multiple diffuse vents within one vent field (Huber et al, 2007;Opatkiewicz et al, 2009;Perner et al, 2010;Akerman et al, 2013;Meier et al, 2016;Olins et al, 2017) show that the microbial community composition is shaped by both the geochemistry as well as the distance between individual diffuse vents. For example, Akerman et al (2013) showed that patterns in abundance of Epsilonbacteraeota at Axial Seamount were correlated to vent methane concentrations as well as vent location, while at the Menez Gwen vent field, Meier et al (2016) found a transition from chemolithoautotrophic communities close to sources of venting to heterotrophic communities with increasing distance from the venting source.…”

Hydrothermal vent protistan distribution along the Mariana arc suggests vent endemics may be rare and novel

“…Chemolithoautotrophic (chemosynthetic) primary production in the deep ocean is most intense in areas around hydrothermal vents, where it is supported by reducing substances formed during hydrothermal circulation through crustal rocks beneath the seafloor (Jannasch and Wirsen, 1979;Karl et al, 1980;Reysenbach and Shock, 2002;Amend et al, 2011;Olins et al, 2017). Global primary production by prokaryotes in subseafloor hydrothermal systems is estimated to be roughly 1.4 Tg C y −1 (McNichol et al, 2018), resulting in hot spots of labile carbon availability around areas of active hydrothermal discharge from the subseafloor.…”