Life and Death of Deep-Sea Vents: Bacterial Diversity and Ecosystem Succession on Inactive Hydrothermal Sulfides

Abstract

ABSTRACT Hydrothermal chimneys are a globally dispersed habitat on the seafloor associated with mid-ocean ridge (MOR) spreading centers. Active, hot, venting sulfide structures from MORs have been examined for microbial diversity and ecology since their discovery in the mid-1970s, and recent work has also begun to explore the microbiology of inactive sulfides—structures that persist for decades to millennia and form moderate to massive deposits at and below the seafloor. Here we used tag pyrosequencing of the V6 region of the 16S rRNA and full-length 16S rRNA sequencing on inactive hydrothermal sulfide chimney samples from 9°N on the East Pacific Rise to learn their bacterial composition, metabolic potential, and succession from venting to nonventing (inactive) regimes. Alpha-, beta-, delta-, and gammaproteobacteria and members of the phylum Bacteroidetes dominate all inactive sulfides. Greater than 26% of the V6 tags obtained are closely related to lineages involved in sulfur, nitrogen, iron, and methane cycling. Epsilonproteobacteria represent <4% of the V6 tags recovered from inactive sulfides and 15% of the full-length clones, despite their high abundance in active chimneys. Members of the phylum Aquificae, which are common in active vents, were absent from both the V6 tags and full-length 16S rRNA data sets. In both analyses, the proportions of alphaproteobacteria, betaproteobacteria, and members of the phylum Bacteroidetes were greater than those found on active hydrothermal sulfides. These shifts in bacterial population structure on inactive chimneys reveal ecological succession following cessation of venting and also imply a potential shift in microbial activity and metabolic guilds on hydrothermal sulfides, the dominant biome that results from seafloor venting. IMPORTANCE Hydrothermal chimneys are globally dispersed seafloor habitats associated with mid-ocean ridge spreading centers. Active, hot, venting chimneys have been examined for microbial ecology since their discovery in the late 1970s, but the microbiology of inactive chimneys, which may persist for thousands of years, has only recently been explored. We studied bacterial diversity on inactive hydrothermal sulfide chimney samples from 9°N on the East Pacific Rise to learn their bacterial community composition, potential ecological roles, and succession from active venting to inactive chimneys. Many bacteria on inactive sulfide chimneys are closely related to lineages involved in sulfur, nitrogen, iron, and methane cycling, and two common groups found on active chimneys are nearly absent from inactive vents, where they were replaced by groups likely involved in the elemental cycling mentioned above. Our findings reveal that ecological succession occurs on hydrothermal sulfides after active venting ceases and also imply a potential shift in microbial metabolic guilds.