Project: Microbial activity in oxygenated subseafloor sediment

The subseafloor sedimentary biosphere is the largest ecosystem on Earth, where microbes subsist under energy-limited conditions over long timescales. It is poorly understood how activity is converted into microbial reproduction and survival under these conditions. Here, we examine this question in deep-sea subseafloor communities subsisting in oxic and anoxic abyssal sediments for over multimillion year timescales. Ammonia-oxidizing Archaea (AOA) dominate oxic abyssal microbial communities by up to an order of magnitude for 15 million years in the oxic subseafloor of the North Atlantic Ocean. Rates of nitrification correlated with the abundance of these dominant AOA populations, whose metabolism is characterized by ammonia oxidation, mixotrophic utilization of organic nitrogen, deamination, and the energetically efficient chemolithoautotrophic hydroxypropionate/ hydroxybutyrate carbon fixation cycle. These AOA thus have the potential to couple mixotrophic and chemolithoautotrophic metabolism via mixotrophic deamination of organic nitrogen, followed by oxidation of the regenerated ammonia for additional energy to fuel carbon fixation. This metabolic feature likely reduces energy loss and improves AOA fitness under energy starved, oxic conditions, thereby allowing them to outcompete other taxa for millions of years. In abyssal anoxic sites, a single population affiliated with the candidate Phylum "Candidatus Atribacteria" dominates the subseafloor community for up to 8 million years. Expression of genes encoding proteins for cell division were detected only in the upper 10 mbsf, indicating increased abundances of "Ca. Atribacteria" were due to actively reproducing microbes. Mean net sulfate reduction rate is relatively high over the upper 10-meter interval. At greater depths, the ecosystem is subject to net death, with mean net sulfate reduction rate below detection, microbial abundance steadily declining, and no detectable expression of cell division genes. Even in this net-death interval, "Ca. Atribacteria" dominates the subseafloor community. The transcriptomes indicate that "Ca. Atribacteria" is homoacetogenic, utilizing electron bifurcation to couple fermentative H2 production from sugars with the Wood-Ljungdahl carbon fixation pathway. Additional reducing power for ATP synthesis appears to be gained by secondary fermentations via a bacterial micro-compartment. This energy-efficient metabolism apparently improves the fitness of "Ca. Atribacteria" in this energy-limited setting, allowing this group to dominate communities over multimillion-year timescales.

Additional project information is available from C-DEBI: https://www.darkenergybiosphere.org/award/microbial-activity-in-oxygenated-subseafloor-sediment/