Abstract
ABSTRACTThe South Pacific Gyre (SPG) possesses the lowest rates of sedimentation, surface chlorophyll concentration, and primary productivity in the global oceans. As a direct result, deep-sea sediments are thin and contain small amounts of labile organic carbon. It was recently shown that the entire SPG sediment column is oxygenated and may be representative of up to a third of the global marine environment. To understand the microbial processes that contribute to the removal of the labile organic matter at the water-sediment interface, a sediment sample was collected and subjected to metagenomic sequencing and analyses. Analysis of nine partially reconstructed environmental genomes, which represent approximately one-third of the microbial community, revealed that the members of the SPG surface sediment microbial community are phylogenetically distinct from surface/upper-ocean organisms. These genomes represent a wide distribution of novel organisms, including deep-branching Alphaproteobacteria, two novel organisms within the Proteobacteria, and new members of the Nitrospirae, Nitrospinae, and candidate phylum NC10. These genomes contain evidence for microbially mediated metal (iron/manganese) oxidation and carbon fixation linked to nitrification. Additionally, despite hypothesized energy limitation, members of the SPG microbial community had motility and chemotaxis genes and possessed mechanisms for the degradation of high-molecular-weight organic matter. This study contributes to our understanding of the metabolic potential of microorganisms in deep-sea oligotrophic sediments and their impact on local carbon geochemistry.IMPORTANCE This research provides insight into the microbial metabolic potential of organisms inhabiting oxygenated deep-sea marine sediments. Current estimates suggest that these environments account for up to a third of the global marine sediment habitat. Nine novel deep-sea microbial genomes were reconstructed from a metagenomic data set and expand the limited number of environmental genomes from deep-sea sediment environments. This research provides phylogeny-linked insight into critical metabolisms, including carbon fixation associated with nitrification, which is assignable to members of the marine group 1 Thaumarchaeota, Nitrospinae, and Nitrospirae and neutrophilic metal (iron/manganese) oxidation assignable to a novel proteobacterium.
Highlights
The South Pacific Gyre (SPG) possesses the lowest rates of sedimentation, surface chlorophyll concentration, and primary productivity in the global oceans
Representative of approximately 36% of the total microbial abundance, were identified from a metagenomic data set sampled from the oxic SPG surface sediments
SPGG8 was related to the Marinimicrobia and Caldithrix as well as a number of other candidate phyla; the placement of SPGG8 suggested that it represents a novel organism
Summary
The South Pacific Gyre (SPG) possesses the lowest rates of sedimentation, surface chlorophyll concentration, and primary productivity in the global oceans. Standing biomass of microorganisms in surface sediments shows that the SPG contains approximately 2 to 4 orders of magnitude fewer cells per unit of volume than previously measured in marine surface sediment habitats [1, 2, 5], suggesting that the SPG sediments are depleted of sufficient organic energy inputs for a robust microbial population relative to highproductivity regions The implication of these carbon-depleted conditions is that there is a direct impact on potential metabolisms and cellular functions of extant microorganisms in the surface sediment environment. It remains unclear whether the microbial community in the SPG surface sediments is composed of oligotrophic organisms, with limited metabolic potential, or copiotrophic organisms that possess a broad metabolic potential and can respond to sporadic organic matter inputs
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