Spatially resolved sampling reveals dynamic microbial communities in rising hydrothermal plumes across a back-arc basin

Abstract

Within hydrothermal plumes, chemosynthetic processes and microbe-mineral interactions drive primary productivity in deep-ocean food webs and may influence transport of elements such as iron. However, the source of microorganisms in plumes and the factors governing how these communities assemble are poorly understood, in part due to lack of data from early stages of plume formation. In this study, we examined microbial community composition of rising hydrothermal plumes from five vent fields along the Eastern Lau Spreading Center. Seafloor and plume microbial communities were significantly dissimilar and shared few phylotypes. Plume communities were highly similar to each other with significant differences in community membership only between Kilo Moana and Mariner, two vents that are separated by extremes in depth, latitude and geochemistry. Systematic sampling of waters surrounding the vents revealed that species richness and phylogenetic diversity was typically highest near the vent orifice, implying mixing of microbial communities from the surrounding habitats. Above-plume background communities were primarily dominated by SAR11, SAR324 and MG-I Archaea, while SUP05, Sulfurovum, Sulfurimonas, SAR324 and Alteromonas were abundant in plume and near-bottom background communities. These results show that the ubiquitous water-column microorganisms populate plume communities, and that the composition of background seawater exerts primary influence on plume community composition, with secondary influence from geochemical and/or physical properties of vents. Many of these pervasive deep-ocean organisms are capable of lithotrophy, suggesting that they are poised to use inorganic electron donors encountered in hydrothermal plumes.

Figure 1

Approximate depth, latitudinal location and general characteristics of hydrothermal vents sampled along the spreading ridge in Lau Basin. Arrows give location of vents with respect to spreading center. Figure inset gives distance in kilometers of each vent relative to one another. The table describes location and previously reported geochemistry of end-member fluids associated with each vent. Bathymetry was generated using GeoMapApp (http://www.geomapapp.org) and plotted in R.

Figure 2

Sampling methodology overview. (a) Operator view of Jason II sampling actively venting fluids with the SUPR sampler. Because no high-resolution pictures of SUPR from ELSC were available, the image shown here is from the Mid Cayman Rise. Jason imagery courtesy of the National Science Foundation, Woods Hole Oceanographic Institution and CR German. (b) Sampling locations relative to the vent orifice are highlighted by yellow circles.

Figure 3

Non-metric multidimensional scaling (NMDS) ordination of Jaccard distances showing similarity of RP (RP), orifice (< 1 m), NBB, APB and sulfide hosted microbial communities (seafloor). Samples are colored by vent field at ELSC. NMDS stress=0.096.

Figure 4

Abundance of dominant Alpha-, Delta-, Epsilon- and Gammaproteobacteria OTUs across all water samples from Lau Basin. The abundance of proteobacterial OTUs₉₇ is designated by color intensity; note that the color scale maximums change with each class to provide definition. Individual filter samples are arranged by Jaccard similarity and represent the entire community and the sampling location designated by symbol and color. Stars indicate potential contaminants.

Figure 5

(a) Abundance of dominant bacterial groups in NBB, orifice, RP (indicated by meters above orifice), and APB. Color, arrangement and size of the circles indicate the identity and abundance of the groups as shown in the legend. Note that in some cases samples from the same vent site were collected on different dives. NS indicates plume heights that were not sampled. Asterisks indicate height at which samples were taken at Mariner. (b) A conceptual model of potential sources of microorganisms within plumes. Solid and dashed arrows denote hypothesized strength of influence (solid arrows=stronger influence; dashed=weaker).