Climate oscillations reflected within the microbiome of Arabian Sea sediments

William D Orsi,Lijun He,Xabier Irigoien,Valier Galy,Mitchell Lee,Marco J L Coolen,Carl Johnson,Guillem Chust,Cornelia Wuchter,Jordon D Hemingway,Liviu Giosan,Kuldeep D More

doi:10.1038/s41598-017-05590-9

Abstract

Selection of microorganisms in marine sediment is shaped by energy-yielding electron acceptors for respiration that are depleted in vertical succession. However, some taxa have been reported to reflect past depositional conditions suggesting they have experienced weak selection after burial. In sediments underlying the Arabian Sea oxygen minimum zone (OMZ), we performed the first metagenomic profiling of sedimentary DNA at centennial-scale resolution in the context of a multi-proxy paleoclimate reconstruction. While vertical distributions of sulfate reducing bacteria and methanogens indicate energy-based selection typical of anoxic marine sediments, 5–15% of taxa per sample exhibit depth-independent stratigraphies indicative of paleoenvironmental selection over relatively short geological timescales. Despite being vertically separated, indicator taxa deposited under OMZ conditions were more similar to one another than those deposited in bioturbated intervals under intervening higher oxygen. The genomic potential for denitrification also correlated with palaeo-OMZ proxies, independent of sediment depth and available nitrate and nitrite. However, metagenomes revealed mixed acid and Entner-Dourdoroff fermentation pathways encoded by many of the same denitrifier groups. Fermentation thus may explain the subsistence of these facultatively anaerobic microbes whose stratigraphy follows changing paleoceanographic conditions. At least for certain taxa, our analysis provides evidence of their paleoenvironmental selection over the last glacial-interglacial cycle.

Highlights

In marine sediment, energy-yielding electron acceptors for microbial respiration are sequentially depleted based on the amount of energy they provide, which is linked to the oxidation of organic matter[1,2,3]
The age model used to determine the timing of changes in depositional and environmental conditions is based on the correlation of our XRFderived bromine (Br) record to the high-resolution total organic carbon (TOC) record of Schulz et al.[20] and radiocarbon dating of foraminiferal carbonates (Tables S1, S2)
In agreement with earlier studies[21, 22, 52], our results show that oxygen minimum zone (OMZ) conditions and denitrification mainly occurred during the warm interstadials, which led to the deposition of δ15N-enriched and TOC-rich (>0.5%) sediments, while no or weak OMZ during cold stadials resulted in the deposition of bioturbated TOC-poor sediments

Summary

Introduction

Energy-yielding electron acceptors for microbial respiration are sequentially depleted based on the amount of energy they provide, which is linked to the oxidation of organic matter[1,2,3]. These include continental mid-Cretaceous black shales harboring marine communities[16], lignite-hosted subseafloor microbiomes that resemble soil communities[14], Mediterranean turbidites harboring increased bacterial taxa from soils[17], bacteria in Baltic Sea sediments that reflect variations in paleo-salinity[18], and correlations between the microbial diversity and past depositional conditions in maar lake sediments[19] These studies imply that such taxa underwent weak selection pressure after burial, either through dormancy or surviving by utilizing less-competitive substrates such as fermentation substrates (compared to higher-energy electron acceptors for respiration). Subsistence under weak selection is a hypothesis that could potentially help explain why some taxa in marine sediments correlate with environmental conditions that prevailed at the time of deposition

Methods

Results

Conclusion