Metagenomic resolution of microbial functions in deep-sea hydrothermal plumes across the Eastern Lau Spreading Center

Abstract

Microbial processes within deep-sea hydrothermal plumes affect ocean biogeochemistry on global scales. In rising hydrothermal plumes, a combination of microbial metabolism and particle formation processes initiate the transformation of reduced chemicals like hydrogen sulfide, hydrogen, methane, iron, manganese and ammonia that are abundant in hydrothermal vent fluids. Despite the biogeochemical importance of this rising portion of plumes, it is understudied in comparison to neutrally buoyant plumes. Here we use metagenomics and bioenergetic modeling to describe the abundance and genetic potential of microorganisms in relation to available electron donors in five different hydrothermal plumes and three associated background deep-sea waters from the Eastern Lau Spreading Center located in the Western Pacific Ocean. Three hundred and thirty one distinct genomic 'bins' were identified, comprising an estimated 951 genomes of archaea, bacteria, eukarya and viruses. A significant proportion of these genomes is from novel microorganisms and thus reveals insights into the energy metabolism of heretofore unknown microbial groups. Community-wide analyses of genes encoding enzymes that oxidize inorganic energy sources showed that sulfur oxidation was the most abundant and diverse chemolithotrophic microbial metabolism in the community. Genes for sulfur oxidation were commonly present in genomic bins that also contained genes for oxidation of hydrogen and methane, suggesting metabolic versatility in these microbial groups. The relative diversity and abundance of genes encoding hydrogen oxidation was moderate, whereas that of genes for methane and ammonia oxidation was low in comparison to sulfur oxidation. Bioenergetic-thermodynamic modeling supports the metagenomic analyses, showing that oxidation of elemental sulfur with oxygen is the most dominant catabolic reaction in the hydrothermal plumes. We conclude that the energy metabolism of microbial communities inhabiting rising hydrothermal plumes is dictated by the underlying plume chemistry, with a dominant role for sulfur-based chemolithoautotrophy.

Genome reduction in an abundant and ubiquitous soil bacterium ‘Candidatus Udaeobacter copiosus’

“…U copiosus genome is ∼94% complete, based on domain-specific single-copy housekeeping genes commonly used to estimate genome completion 23 (Supplementary Table 3). This list of single-copy genes has been used to estimate genome completeness in several recent studies 13,63 . When we analysed the genome using another metric of genome completeness (checkM 64 ), the results suggested that the genome was 80% complete with 4% contamination, a level categorized as a 'substantially complete draft with low contamination'.…”

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

“…In addition, a study within a single vent field at Axial Seamount showed differences in gene expression patterns between both diffuse vents as well as within the intra‐field waters between vent sites (Olins et al ., ). Finally, through the reconstruction of genomes from metagenomes (Tyson et al ., ; Dick et al ., ; Hug et al ., ), recent genomic binning studies at hydrothermal systems have revealed the presence of novel microbial and viral groups as well as their metabolic potential, including the discovery of auxiliary metabolic genes for sulfur oxidation within deep ocean viruses and the potential importance of hydrocarbon degradation distal to venting fluids, including within hydrothermal plumes (Anantharaman et al ., ; Li et al ., ; Sheik et al ., ; Meier et al ., ).…”

High potential for temperate viruses to drive carbon cycling in chemoautotrophy‐dominated shallow‐water hydrothermal vents

“…This process is consistent with experimental evidence and theoretical models indicating that viral lysis can enhance carbon cycling and nutrient regeneration within the microbial loop (Middelboe et al ., ; Poorvin et al ., ; Weinbauer et al ., ; Shelford et al ., ; Weitz et al ., ). Recent studies suggest a tight coupling between chemoautotrophic and HCP in deep‐sea hydrothermal vent ecosystems (Bennett et al ., ), and viruses infecting the dominant chemoautotrophs have been inferred as a possible link between primary and secondary production processes in such systems (Anantharaman et al ., 2014, 2016; Li et al ., ). To our knowledge, we present here the first experimental evidence supporting the hypothesis that provirus‐host interactions can profoundly influence the carbon cycling in hydrothermal vents, opening novel research perspectives on these dynamics.…”