Environmental Conditions Outweigh Geographical Contiguity in Determining the Similarity of nifH-Harboring Microbial Communities in Sediments of Two Disconnected Marginal Seas.

Haixia Zhou,Martin G Klotz,Hongyue Dang

doi:10.3389/fmicb.2016.01111

Abstract

Ecological evidence suggests that heterotrophic diazotrophs fueled by organic carbon respiration in sediments play an important role in marine nitrogen fixation. However, fundamental knowledge about the identities, abundance, diversity, biogeography, and controlling environmental factors of nitrogen-fixing communities in open ocean sediments is still elusive. Surprisingly, little is known also about nitrogen-fixing communities in sediments of the more research-accessible marginal seas. Here we report on an investigation of the environmental geochemistry and putative diazotrophic microbiota in the sediments of Bohai Sea, an eutrophic marginal sea of the western Pacific Ocean. Diverse and abundant nifH gene sequences were identified and sulfate-reducing bacteria (SRB) were found to be the dominant putative nitrogen-fixing microbes. Community statistical analyses suggested bottom water temperature, bottom water chlorophyll a content (or the covarying turbidity) and sediment porewater Eh (or the covarying pH) as the most significant environmental factors controlling the structure and spatial distribution of the putative diazotrophic communities, while sediment Hg content, sulfide content, and porewater -Si content were identified as the key environmental factors correlated positively with the nifH gene abundance in Bohai Sea sediments. Comparative analyses between the Bohai Sea and the northern South China Sea (nSCS) identified a significant composition difference of the putative diazotrophic communities in sediments between the shallow-water (estuarine and nearshore) and deep-water (offshore and deep-sea) environments, and sediment porewater dissolved oxygen content, water depth and in situ temperature as the key environmental factors tentatively controlling the species composition, community structure, and spatial distribution of the marginal sea sediment nifH-harboring microbiota. This confirms the ecophysiological specialization and niche differentiation between the shallow-water and deep-water sediment diazotrophic communities and suggests that the in situ physical and geochemical conditions play a more important role than geographical contiguity in determining the community similarity of the diazotrophic microbiota in marginal sea sediments.

Highlights

N2-fixing prokaryotes play a key role in marine nitrogen (N) cycling and ecosystem functioning such as carbon sequestration by providing newly fixed nitrogenous nutrients, important in oligotrophic environments of the ocean (Karl et al, 1997; Dore et al, 2002; Montoya et al, 2004; Steppe and Paerl, 2005; Karl and Letelier, 2008; Sohm et al, 2011)
Nitrogenous nutrient-rich environments such as estuarine and coastal seawaters and marine sediments have long been regarded as environments lacking significant diazotrophic activities, inferred previously from bacterial culture-based
This inferred popular opinion resulted in a long-time negligence of the N2-fixing microorganisms and activities in these environments whereas newer work led to the hypothesis that marginal sea sediments may instead harbor diverse and abundant N2-fixing microorganisms (Knapp, 2012; Bertics et al, 2013; Dang et al, 2013a; Dekaezemacker et al, 2013; Voss et al, 2013)

Summary

Introduction

N2-fixing prokaryotes play a key role in marine nitrogen (N) cycling and ecosystem functioning such as carbon sequestration by providing newly fixed nitrogenous nutrients, important in oligotrophic environments of the ocean (Karl et al, 1997; Dore et al, 2002; Montoya et al, 2004; Steppe and Paerl, 2005; Karl and Letelier, 2008; Sohm et al, 2011). The marine N cycle appears to be a conundrum because the estimated N input by N2 fixation is significantly lower than the estimated N loss via denitrification and anaerobic ammonium oxidation (anammox) (Mahaffey et al, 2005). This suggested that the inventory of reactive nitrogen in the oceans is unbalanced and dwindling (Moisander et al, 2014). This conundrum may be an artifact caused by uncertainties in previous research results and underestimations of N2-fixation contribution to the marine N budget. The recent detection of numerous diazotrophic bacteria and archaea in marine sediments led to the hypothesis that marine sediments might constitute an important environment for N2 fixation in the oceans (Pernthaler et al, 2008; Dang et al, 2009a, 2013a; Dekas et al, 2009, 2014, 2016; Fulweiler, 2009; Miyazaki et al, 2009)

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