A Nanoscale Study of Carbon and Nitrogen Fluxes in Mats of Purple Sulfur Bacteria: Implications for Carbon Cycling at the Surface of Coastal Sediments.

Cédric Hubas,Cédric Hubas,Cédric Hubas,Christian Jeanthon,Christian Jeanthon,Christian Jeanthon,Christian Jeanthon,Yann Bozec,Yann Bozec,Yann Bozec,Yann Bozec,Najet Thiney,Najet Thiney,Najet Thiney,Najet Thiney,Dominique Boeuf,Bruno Jesus,Bruno Jesus

doi:10.3389/fmicb.2017.01995

Abstract

Mass blooms of purple sulfur bacteria growing seasonally on green stranded macroalgae have a major impact on the microbial composition and functionality of intertidal mats. To explore the active anoxygenic phototrophic community in purple bacterial mats from the Roscoff Aber Bay (Brittany, France), we conducted a combined approach including molecular and high-resolution secondary ion mass spectrometry (NanoSIMS) analyses. To investigate the dynamics of carbon and nitrogen assimilation activities, NanoSIMS was coupled with a stable isotope probing (SIP) experiment and a compound specific isotope analysis (CSIA) of fatty acid methyl ester (FAME). Sediment samples were incubated with 13C- and/or 15N-labeled acetate, pyruvate, bicarbonate and ammonium. NanoSIMS analysis of 13C - and 15N -incubated samples showed elevated incorporations of 13C - and 15N in the light and of 13C -acetate in the dark into dense populations of spherical cells that unambiguously dominated the mats. These results confirmed CSIA data that ranked vaccenic acid, an unambiguous marker of purple sulfur bacteria, as the most strongly enriched in the light after 13C -acetate amendment and indicated that acetate uptake, the most active in the mat, was not light-dependent. Analysis of DNA- and cDNA-derived pufM gene sequences revealed that Thiohalocapsa-related clones dominated both libraries and were the most photosynthetically active members of the mat samples. This study provides novel insights into the contribution of purple sulfur bacteria to the carbon cycle during their seasonal developments at the sediment surface in the intertidal zone.

Highlights

Microbial mats are complex small-scale self-sustaining benthic ecosystems (Stal, 1985) often built by cyanobacteria whose primary production enrich the sediment with organic matter that becomes available to different functional groups of microorganisms
We suggested that photosynthetic efficiency was probably hampered in these mats and that macroalgal-derived organic matter favored the photoheterotrophic lifestyle of purple sulfur bacteria
The mats were characterized by several bacterial markers such as branched Fatty acids (FAs), two cyclopropane FAs, as well as the vaccenic fatty acid (C18:1n-7)

Summary

Introduction

Microbial mats are complex small-scale self-sustaining benthic ecosystems (Stal, 1985) often built by cyanobacteria whose primary production enrich the sediment with organic matter that becomes available to different functional groups of microorganisms. We previously assessed the biochemical composition (fatty acids, photosynthetic pigments) of the microbial mats and their influence on ecosystem functions (sediment cohesiveness, CO2 fixation) at low tide in Roscoff Aber Bay and demonstrated that the proliferation of these purple sulfur bacteria have a major impact on the diversity and functionality of intertidal mats (Hubas et al, 2013) Their massive growth resulted in a dramatic increase of both gross CO2 fixation as well as total mat respiration in comparison to diatom-dominated mats. We suggested that photosynthetic efficiency was probably hampered in these mats and that macroalgal-derived organic matter favored the photoheterotrophic lifestyle of purple sulfur bacteria

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