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

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),...

Full description

Bibliographic Details
Main Authors: Cédric Hubas, Dominique Boeuf, Bruno Jesus, Najet Thiney, Yann Bozec, Christian Jeanthon
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-10-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fmicb.2017.01995/full
id doaj-3098eb78ef9744f1934fe63b0c807390
record_format Article
spelling doaj-3098eb78ef9744f1934fe63b0c8073902020-11-24T23:14:28ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-10-01810.3389/fmicb.2017.01995299926A Nanoscale Study of Carbon and Nitrogen Fluxes in Mats of Purple Sulfur Bacteria: Implications for Carbon Cycling at the Surface of Coastal SedimentsCédric Hubas0Dominique Boeuf1Dominique Boeuf2Bruno Jesus3Bruno Jesus4Najet Thiney5Yann Bozec6Yann Bozec7Christian Jeanthon8Christian Jeanthon9Muséum National d’Histoire Naturelle, UMR BOREA, MNHN-CNRS-UCN-UPMC-IRD-UA, Station de Biologie Marine de Concarneau, Concarneau, FranceCNRS, Station Biologique de Roscoff, Adaptation et Diversité en Milieu Marin, Roscoff, FranceSorbonne Universités, UPMC Univ Paris 06, UMR 7144, Station Biologique de Roscoff, Adaptation et Diversité en Milieu Marin, Roscoff, FranceEA2160, Laboratoire Mer Molécules Santé, Université de Nantes, Nantes, FranceBioISI – Biosystems & Integrative Sciences Institute, Campo Grande University of Lisbon, Faculty of Sciences, Lisbon, PortugalMuséum National d’Histoire Naturelle, UMR BOREA, MNHN-CNRS-UCN-UPMC-IRD-UA, Bâtiment Arthropodes, Paris, FranceCNRS, Station Biologique de Roscoff, Adaptation et Diversité en Milieu Marin, Roscoff, FranceSorbonne Universités, UPMC Univ Paris 06, UMR 7144, Station Biologique de Roscoff, Adaptation et Diversité en Milieu Marin, Roscoff, FranceCNRS, Station Biologique de Roscoff, Adaptation et Diversité en Milieu Marin, Roscoff, FranceSorbonne Universités, UPMC Univ Paris 06, UMR 7144, Station Biologique de Roscoff, Adaptation et Diversité en Milieu Marin, Roscoff, FranceMass 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.http://journal.frontiersin.org/article/10.3389/fmicb.2017.01995/fullmicrobial matsChromatiaceaeThiohalocapsastable isotope probing (SIP)NanoSIMScompound specific isotope analysis (CSIA)
collection DOAJ
language English
format Article
sources DOAJ
author Cédric Hubas
Dominique Boeuf
Dominique Boeuf
Bruno Jesus
Bruno Jesus
Najet Thiney
Yann Bozec
Yann Bozec
Christian Jeanthon
Christian Jeanthon
spellingShingle Cédric Hubas
Dominique Boeuf
Dominique Boeuf
Bruno Jesus
Bruno Jesus
Najet Thiney
Yann Bozec
Yann Bozec
Christian Jeanthon
Christian Jeanthon
A Nanoscale Study of Carbon and Nitrogen Fluxes in Mats of Purple Sulfur Bacteria: Implications for Carbon Cycling at the Surface of Coastal Sediments
Frontiers in Microbiology
microbial mats
Chromatiaceae
Thiohalocapsa
stable isotope probing (SIP)
NanoSIMS
compound specific isotope analysis (CSIA)
author_facet Cédric Hubas
Dominique Boeuf
Dominique Boeuf
Bruno Jesus
Bruno Jesus
Najet Thiney
Yann Bozec
Yann Bozec
Christian Jeanthon
Christian Jeanthon
author_sort Cédric Hubas
title A Nanoscale Study of Carbon and Nitrogen Fluxes in Mats of Purple Sulfur Bacteria: Implications for Carbon Cycling at the Surface of Coastal Sediments
title_short A Nanoscale Study of Carbon and Nitrogen Fluxes in Mats of Purple Sulfur Bacteria: Implications for Carbon Cycling at the Surface of Coastal Sediments
title_full A Nanoscale Study of Carbon and Nitrogen Fluxes in Mats of Purple Sulfur Bacteria: Implications for Carbon Cycling at the Surface of Coastal Sediments
title_fullStr A Nanoscale Study of Carbon and Nitrogen Fluxes in Mats of Purple Sulfur Bacteria: Implications for Carbon Cycling at the Surface of Coastal Sediments
title_full_unstemmed A Nanoscale Study of Carbon and Nitrogen Fluxes in Mats of Purple Sulfur Bacteria: Implications for Carbon Cycling at the Surface of Coastal Sediments
title_sort nanoscale study of carbon and nitrogen fluxes in mats of purple sulfur bacteria: implications for carbon cycling at the surface of coastal sediments
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2017-10-01
description 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.
topic microbial mats
Chromatiaceae
Thiohalocapsa
stable isotope probing (SIP)
NanoSIMS
compound specific isotope analysis (CSIA)
url http://journal.frontiersin.org/article/10.3389/fmicb.2017.01995/full
work_keys_str_mv AT cedrichubas ananoscalestudyofcarbonandnitrogenfluxesinmatsofpurplesulfurbacteriaimplicationsforcarboncyclingatthesurfaceofcoastalsediments
AT dominiqueboeuf ananoscalestudyofcarbonandnitrogenfluxesinmatsofpurplesulfurbacteriaimplicationsforcarboncyclingatthesurfaceofcoastalsediments
AT dominiqueboeuf ananoscalestudyofcarbonandnitrogenfluxesinmatsofpurplesulfurbacteriaimplicationsforcarboncyclingatthesurfaceofcoastalsediments
AT brunojesus ananoscalestudyofcarbonandnitrogenfluxesinmatsofpurplesulfurbacteriaimplicationsforcarboncyclingatthesurfaceofcoastalsediments
AT brunojesus ananoscalestudyofcarbonandnitrogenfluxesinmatsofpurplesulfurbacteriaimplicationsforcarboncyclingatthesurfaceofcoastalsediments
AT najetthiney ananoscalestudyofcarbonandnitrogenfluxesinmatsofpurplesulfurbacteriaimplicationsforcarboncyclingatthesurfaceofcoastalsediments
AT yannbozec ananoscalestudyofcarbonandnitrogenfluxesinmatsofpurplesulfurbacteriaimplicationsforcarboncyclingatthesurfaceofcoastalsediments
AT yannbozec ananoscalestudyofcarbonandnitrogenfluxesinmatsofpurplesulfurbacteriaimplicationsforcarboncyclingatthesurfaceofcoastalsediments
AT christianjeanthon ananoscalestudyofcarbonandnitrogenfluxesinmatsofpurplesulfurbacteriaimplicationsforcarboncyclingatthesurfaceofcoastalsediments
AT christianjeanthon ananoscalestudyofcarbonandnitrogenfluxesinmatsofpurplesulfurbacteriaimplicationsforcarboncyclingatthesurfaceofcoastalsediments
AT cedrichubas nanoscalestudyofcarbonandnitrogenfluxesinmatsofpurplesulfurbacteriaimplicationsforcarboncyclingatthesurfaceofcoastalsediments
AT dominiqueboeuf nanoscalestudyofcarbonandnitrogenfluxesinmatsofpurplesulfurbacteriaimplicationsforcarboncyclingatthesurfaceofcoastalsediments
AT dominiqueboeuf nanoscalestudyofcarbonandnitrogenfluxesinmatsofpurplesulfurbacteriaimplicationsforcarboncyclingatthesurfaceofcoastalsediments
AT brunojesus nanoscalestudyofcarbonandnitrogenfluxesinmatsofpurplesulfurbacteriaimplicationsforcarboncyclingatthesurfaceofcoastalsediments
AT brunojesus nanoscalestudyofcarbonandnitrogenfluxesinmatsofpurplesulfurbacteriaimplicationsforcarboncyclingatthesurfaceofcoastalsediments
AT najetthiney nanoscalestudyofcarbonandnitrogenfluxesinmatsofpurplesulfurbacteriaimplicationsforcarboncyclingatthesurfaceofcoastalsediments
AT yannbozec nanoscalestudyofcarbonandnitrogenfluxesinmatsofpurplesulfurbacteriaimplicationsforcarboncyclingatthesurfaceofcoastalsediments
AT yannbozec nanoscalestudyofcarbonandnitrogenfluxesinmatsofpurplesulfurbacteriaimplicationsforcarboncyclingatthesurfaceofcoastalsediments
AT christianjeanthon nanoscalestudyofcarbonandnitrogenfluxesinmatsofpurplesulfurbacteriaimplicationsforcarboncyclingatthesurfaceofcoastalsediments
AT christianjeanthon nanoscalestudyofcarbonandnitrogenfluxesinmatsofpurplesulfurbacteriaimplicationsforcarboncyclingatthesurfaceofcoastalsediments
_version_ 1725594225122213888