Relationship of Bacterial Richness to Organic Degradation Rate and Sediment Age in Subseafloor Sediment.

Emily A Walsh,Arthur J Spivack,Richard W Murray,Steven D'Hondt,Mitchell L Sogin,John B Kirkpatrick,Justine Sauvage,Robert Pockalny

doi:10.1128/aem.00809-16

Abstract

ABSTRACTSubseafloor sediment hosts a large, taxonomically rich, and metabolically diverse microbial ecosystem. However, the factors that control microbial diversity in subseafloor sediment have rarely been explored. Here, we show that bacterial richness varies with organic degradation rate and sediment age. At three open-ocean sites (in the Bering Sea and equatorial Pacific) and one continental margin site (Indian Ocean), richness decreases exponentially with increasing sediment depth. The rate of decrease in richness with increasing depth varies from site to site. The vertical succession of predominant terminal electron acceptors correlates with abundance-weighted community composition but does not drive the vertical decrease in richness. Vertical patterns of richness at the open-ocean sites closely match organic degradation rates; both properties are highest near the seafloor and decline together as sediment depth increases. This relationship suggests that (i) total catabolic activity and/or electron donor diversity exerts a primary influence on bacterial richness in marine sediment and (ii) many bacterial taxa that are poorly adapted for subseafloor sedimentary conditions are degraded in the geologically young sediment, where respiration rates are high. Richness consistently takes a few hundred thousand years to decline from near-seafloor values to much lower values in deep anoxic subseafloor sediment, regardless of sedimentation rate, predominant terminal electron acceptor, or oceanographic context.IMPORTANCE Subseafloor sediment provides a wonderful opportunity to investigate the drivers of microbial diversity in communities that may have been isolated for millions of years. Our paper shows the impact of in situ conditions on bacterial community structure in subseafloor sediment. Specifically, it shows that bacterial richness in subseafloor sediment declines exponentially with sediment age, and in parallel with organic-fueled oxidation rate. This result suggests that subseafloor diversity ultimately depends on electron donor diversity and/or total community respiration. This work studied how and why biological richness changes over time in the extraordinary ecosystem of subseafloor sediment.

Highlights

Subseafloor sediment hosts a large, taxonomically rich, and metabolically diverse microbial ecosystem
The rate of decrease in richness with depth varies greatly from site to site; OTU richness approaches low relatively stable values several tens of meters below the seafloor at site U1343 but within a couple of meters below seafloor at site EQP8. This exponential decline in richness occurs at every phylogenetic level: whether defined by similarity as high as 100% or as low as 85%, the number of operational taxonomic units in normalized samples declines with increasing sediment depth
The lack of clear correspondence between bacterial richness and redox zonation suggests that the predominant terminal electron-accepting pathway does not exert primary control on OTU richness of subseafloor bacterial communities

Summary

Introduction

Subseafloor sediment hosts a large, taxonomically rich, and metabolically diverse microbial ecosystem. Vertical patterns of richness at the open-ocean sites closely match organic degradation rates; both properties are highest near the seafloor and decline together as sediment depth increases This relationship suggests that (i) total catabolic activity and/or electron donor diversity exerts a primary influence on bacterial richness in marine sediment and (ii) many bacterial taxa that are poorly adapted for subseafloor sedimentary conditions are degraded in the geologically young sediment, where respiration rates are high. It shows that bacterial richness in subseafloor sediment declines exponentially with sediment age, and in parallel with organic-fueled oxidation rate This result suggests that subseafloor diversity depends on electron donor diversity and/or total community respiration. To document microbial diversity and its potential drivers in subseafloor sediment, we extracted and sequenced PCR amplicons for the V4 to V6 hypervariable region of the bacterial 16S rRNA gene from the sediment of four distinct locations: the Bering Sea (Integrated Ocean Drilling Program [IODP] expedition 323 site U1343) [13], the eastern equatorial Pacific (Knorr expedition 195-3 site EQP1), the central equatorial Pacific Ocean (Knorr 195-3 site EQP8), and the Bay of Bengal continental margin (Indian National Gas Hydrate Program [NGHP] site NGHP1-14) [14] (Fig. 1)

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Conclusion