Skip to main content
OSTI.GOVU.S. Department of Energy Office of Scientific and Technical Information
U.S. Department of Energy
Office of Scientific and Technical Information
 

Microscale sulfur cycling in the phototrophic pink berry consortia of the Sippewissett Salt Marsh: Sulfur cycling in pink berries of the Sippewissett Marsh

Journal Article · · Environmental Microbiology
 [1];  [2];  [3];  [4];  [5];  [6];  [7];  [8];  [9];  [10];  [11]
  1. Univ. of California, Davis, CA (United States). Dept. of Microbiology Graduate Group; DOE/OSTI
  2. Shell Technology Norway, Oslo (Norway). Arctic Technology; Harvard Univ., Cambridge, MA (United States). Dept. of Organismic and Evolutionary Biology
  3. Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Marine Sciences
  4. Univ. of Arizona, Tucson, AZ (United States). Ecology and Evolutionary Biology
  5. Univ. of California, Davis, CA (United States). Dept. of Evolution and Ecology; Univ. of California, Davis, CA (United States). Dept. of Microbiology and Immunology; Univ. of California, Davis, CA (United States). UC Davis Genome Center
  6. Univ. of California, Davis, CA (United States). UC Davis Genome Center; Univ. of California, Davis, CA (United States). Dept. of Biomedical Engineering
  7. Cornell Univ., Ithaca, NY (United States). Crop and Soil Sciences
  8. Cornell Univ., Ithaca, NY (United States). Dept. of Microbiology
  9. Indiana Univ.--Purdue Univ., Indianapolis, IN (United States). Dept. of Earth Sciences
  10. Washington University, St. Louis, MO (United States). Dept. of Earth and Planetary Sciences
  11. California Institute of Technology (CalTech), Pasadena, CA (United States). Division of Geological and Planetary Sciences
+ Show Author Affiliations

Microbial metabolism is the engine that drives global biogeochemical cycles, yet many key transformations are carried out by microbial consortia over short spatiotemporal scales that elude detection by traditional analytical approaches. We investigate syntrophic sulfur cycling in the ‘pink berry’ consortia of the Sippewissett Salt Marsh through an integrative study at the microbial scale. The pink berries are macroscopic, photosynthetic microbial aggregates composed primarily of two closely associated species: sulfide-oxidizing purple sulfur bacteria (PB-PSB1) and sulfate-reducing bacteria (PB-SRB1). Using metagenomic sequencing and 34S-enriched sulfate stable isotope probing coupled with nanoSIMS, we demonstrate interspecies transfer of reduced sulfur metabolites from PB-SRB1 to PB-PSB1. The pink berries catalyse net sulfide oxidation and maintain internal sulfide concentrations of 0–500 M. Sulfide within the berries, captured on silver wires and analysed using secondary ion mass spectrometer, increased in abundance towards the berry interior, while δ34S-sulfide decreased from 6‰ to -31‰ from the exterior to interior of the berry. These values correspond to sulfate–sulfide isotopic fractionations (15–53‰) consistent with either sulfate reduction or a mixture of reductive and oxidative metabolisms. Together this combined metagenomic and high-resolution isotopic analysis demonstrates active sulfur cycling at the microscale within well-structured macroscopic consortia consisting of sulfide-oxidizing anoxygenic phototrophs and sulfate-reducing bacteria.

Research Organization:
Marine Biological Laboratory, Woods Hole, MA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
Grant/Contract Number:
FG02-85ER13361
OSTI ID:
1625847
Journal Information:
Environmental Microbiology, Journal Name: Environmental Microbiology Journal Issue: 11 Vol. 16; ISSN 1462-2912
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English

References (95)

Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms journal January 1993
On the ATP generation by Chromatium in darkness journal January 1968
Phototrophic consortia: model systems for symbiotic interrelations between prokaryotes journal March 2002
Biogeochemical cycles of carbon, sulfur, and free oxygen in a microbial mat journal August 1993
Isotope effects associated with the anaerobic oxidation of sulfide by the purple photosynthetic bacterium, Chromatium vinosum journal May 1984
A paired sulfate–pyrite δ34S approach to understanding the evolution of the Ediacaran–Cambrian sulfur cycle journal June 2008
Reaction–diffusion model of nutrient uptake in a biofilm: Theory and experiment journal November 2011
Methods for unveiling cryptic microbial partnerships in nature journal June 2009
Improved 16S rRNA-targeted probe set for analysis of sulfate-reducing bacteria by fluorescence in situ hybridization journal June 2007
Sulfur isotope fractionation during bacterial reduction and disproportionation of thiosulfate and sulfite journal August 1998
A fast and simple turbidimetric method for the determination of sulfate in sulfate-reducing bacterial cultures journal August 2000
The Domain-specific Probe EUB338 is Insufficient for the Detection of all Bacteria: Development and Evaluation of a more Comprehensive Probe Set journal September 1999
Development of a Gold Amalgam Voltammetric Microelectrode for the Determination of Dissolved Fe, Mn, O2, and S(-II) in Porewaters of Marine and Freshwater Sediments journal March 1995
Microbial Architecture of Environmental Sulfur Processes: A Novel Syntrophic Sulfur-Metabolizing Consortia journal December 2009
A marine microbial consortium apparently mediating anaerobic oxidation of methane journal October 2000
Endosymbiotic sulphate-reducing and sulphide-oxidizing bacteria in an oligochaete worm journal May 2001
Late Proterozoic rise in atmospheric oxygen concentration inferred from phylogenetic and sulphur-isotope studies journal July 1996
Anoxic carbon flux in photosynthetic microbial mats as revealed by metatranscriptomics journal November 2012
Ediacaran oxidation and biotic evolution journal November 2007
Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments journal May 2002
Influence of sulfate reduction rates on the Phanerozoic sulfur isotope record journal June 2013
Microbiological disproportionation of inorganic sulfur compounds journal August 2008
Microbial Species Richness and Metabolic Activities in Hypersaline Microbial Mats: Insight into Biosignature Formation Through Lithification journal November 2009
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models journal August 2006
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth journal April 2012
Thiohalocapsa marina sp. nov., from an Indian marine aquaculture pond journal July 2009
Adaptive seeds tame genomic sequence comparison journal January 2011
Metabolic strategies of free-living and aggregate-associated bacterial communities inferred from biologic and chemical profiles in the Black Sea suboxic zone journal September 2011
Microbial interactions involving sulfur bacteria: implications for the ecology and evolution of bacterial communities journal December 2000
The Microbial Engines That Drive Earth's Biogeochemical Cycles journal May 2008
Potential for Chemolithoautotrophy Among Ubiquitous Bacteria Lineages in the Dark Ocean journal September 2011
Large Sulfur Isotope Fractionation Does Not Require Disproportionation journal June 2011
Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla journal September 2012
Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. journal January 1990
Elemental Sulfur and Thiosulfate Disproportionation by Desulfocapsa sulfoexigens sp. nov., a New Anaerobic Bacterium Isolated from Marine Surface Sediment journal January 1998
Characterization, Seasonal Occurrence, and Diel Fluctuation of Poly(hydroxyalkanoate) in Photosynthetic Microbial Mats journal October 2000
Microscale observations of sulfate reduction: Correlation of microbial activity with lithified micritic laminae in modern marine stromatolites journal January 2000
Isotope fractionation by sulfate-reducing natural populations and the isotopic composition of sulfide in marine sediments journal January 2001
How to overcome inter-electrode variability and instability to quantify dissolved oxygen, Fe(II), mn(II), and S(−II) in undisturbed soils and sediments using voltammetry journal June 2012
The metagenomics RAST server – a public resource for the automatic phylogenetic and functional analysis of metagenomes journal September 2008
Community-wide analysis of microbial genome sequence signatures journal January 2009
Complete genome sequence of Desulfocapsa sulfexigens, a marine deltaproteobacterium specialized in disproportionating inorganic sulfur compounds journal April 2013
Isotope fractionation and sulfur metabolism by pure and enrichment cultures of elemental sulfur-disproportionating bacteria journal March 1998
pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree preprint January 2010
PhyloSift: phylogenetic analysis of genomes and metagenomes journal January 2014
Bacterial Sulfur Globules: Occurrence, Structure and Metabolism book January 2006
Inorganic Sulfur Compounds as Electron Donors in Purple Sulfur Bacteria book January 2008
Evolution and Ecology of Microbes Dissimilating Sulfur Compounds: Insights from Siroheme Sulfite Reductases book January 2008
On the ATP generation by Chromatium in darkness journal January 1968
Integrating microbial ecology into ecosystem models: challenges and priorities journal September 2011
The mechanism of the bacterial reduction of sulphate and of sulphite from isotope fractionation studies journal January 1968
Biogeochemical cycles of carbon, sulfur, and free oxygen in a microbial mat journal August 1993
Raman spectroscopic and laser scanning confocal microscopic analysis of sulfur in living sulfur-precipitating marine bacteria journal October 2001
Sulfate reduction and methanogenesis in a Thioploca-dominated sediment off the coast of Chile journal August 1997
Sulfur isotope fractionation during bacterial reduction and disproportionation of thiosulfate and sulfite journal August 1998
A fast and simple turbidimetric method for the determination of sulfate in sulfate-reducing bacterial cultures journal August 2000
Phylogenetic Oligodeoxynucleotide Probes for the Major Subclasses of Proteobacteria: Problems and Solutions journal December 1992
The Domain-specific Probe EUB338 is Insufficient for the Detection of all Bacteria: Development and Evaluation of a more Comprehensive Probe Set journal September 1999
An improved fluorescence in situ hybridization protocol for the identification of bacteria and archaea in marine sediments journal November 2004
Mathematical simulation of the diel O, S, and C biogeochemistry of a hypersaline microbial mat journal May 2005
Fractionation of multiple sulfur isotopes during phototrophic oxidation of sulfide and elemental sulfur by a green sulfur bacterium journal January 2009
The effect of sulfate concentration on (sub)millimeter-scale sulfide δ34S in hypersaline cyanobacterial mats over the diurnal cycle journal October 2009
A cryptic sulfur cycle driven by iron in the methane zone of marine sediment (Aarhus Bay, Denmark) journal June 2011
Effect of electron donors on the fractionation of sulfur isotopes by a marine Desulfovibrio sp. journal August 2011
Sulfate reducing bacteria in microbial mats: Changing paradigms, new discoveries journal March 2006
Characterization of the cys gene locus from Allochromatium vinosum indicates an unusual sulfate assimilation pathway* journal January 2000
Micron-scale mapping of sulfur cycling across the oxycline of a cyanobacterial mat: a paired nanoSIMS and CARD-FISH approach journal June 2008
Oxidation of the Ediacaran Ocean journal December 2006
Zero-valent sulphur is a key intermediate in marine methane oxidation journal November 2012
Resistance, resilience, and redundancy in microbial communities journal August 2008
Pan-genome of the dominant human gut-associated archaeon, Methanobrevibacter smithii, studied in twins journal February 2011
Microbiological Fractionation of Sulphur Isotopes journal February 1964
Reverse dissimilatory sulfite reductase as phylogenetic marker for a subgroup of sulfur-oxidizing prokaryotes journal February 2009
Microbial metatranscriptomics in a permanent marine oxygen minimum zone: OMZ community gene expression journal January 2011
Physiology of purple sulfur bacteria forming macroscopic aggregates in Great Sippewissett Salt Marsh, Massachusetts journal August 1993
Methane and sulfate profiles within the subsurface of a tidal flat are reflected by the distribution of sulfate-reducing bacteria and methanogenic archaea: Sulfate reducers and methanogens in tidal flats journal March 2007
Spatial and temporal variability in a stratified hypersaline microbial mat community: Community variability in hypersaline microbial mat journal April 2009
Isotope effects associated with the anaerobic oxidation of sulfide by the purple photosynthetic bacterium, Chromatium vinosum journal May 1984
Isotope effects associated with the anaerobic oxidation of sulfite and thiosulfate by the photosynthetic bacterium, Chromatium vinosum journal May 1985
Metagenome of a Versatile Chemolithoautotroph from Expanding Oceanic Dead Zones journal October 2009
A Cryptic Sulfur Cycle in Oxygen-Minimum-Zone Waters off the Chilean Coast journal November 2010
Elemental Sulfur and Thiosulfate Disproportionation by Desulfocapsa sulfoexigens sp. nov., a New Anaerobic Bacterium Isolated from Marine Surface Sediment journal January 1998
Characterization, Seasonal Occurrence, and Diel Fluctuation of Poly(hydroxyalkanoate) in Photosynthetic Microbial Mats journal October 2000
Microscale observations of sulfate reduction: Correlation of microbial activity with lithified micritic laminae in modern marine stromatolites journal January 2000
Isotope fractionation by sulfate-reducing natural populations and the isotopic composition of sulfide in marine sediments journal January 2001
Neoproterozoic sulfur isotopes, the evolution of microbial sulfur species, and the burial efficiency of sulfide as sedimentary pyrite journal January 2005
pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree journal October 2010
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments journal March 2010
Segmentation of Multi-Isotope Imaging Mass Spectrometry Data for Semi-Automatic Detection of Regions of Interest journal February 2012
12. Biogeochemistry of Sulfur Isotopes book January 2001
Microbial Stress-Response Physiology and its Implications for Ecosystem Function journal June 2007
Spectrophotometric Determination Of Hydrogen Sulfide In Natural Waters journal May 1969
Microelectrode studies of the photosynthesis and O 2 , H 2 S, and pH profiles of a microbial mat1: O 2 , H 2 S, and pH in microbial mat journal November 1983
Draft genomes from uncultured Thiohalocapsa sp. PB-PSB1 and uncultured Desulfofustis sp. PB-SRB1 from the study "Microscale sulfur cycling in the pink berry consortia of the Sippewissett salt marsh" dataset January 2013
Draft genomes from uncultured Thiohalocapsa sp. PB-PSB1 and uncultured Desulfofustis sp. PB-SRB1 from the study "Microscale sulfur cycling in the pink berry consortia of the Sippewissett salt marsh" dataset January 2013

Cited By (19)

Role of bacteria in the production and degradation of Microcystis cyanopeptides journal February 2016
Microbial interactions and community assembly at microscales journal June 2016
Structural basis for allosteric transitions of a multidomain pentameric ligand-gated ion channel journal June 2020
Insights into the single cell draft genome of "Candidatus Achromatium palustre" text January 2016
Stable Isotope Phenotyping via Cluster Analysis of NanoSIMS Data As a Method for Characterizing Distinct Microbial Ecophysiologies and Sulfur-Cycling in the Environment journal May 2016
Metagenomic Reconstruction of Key Anaerobic Digestion Pathways in Municipal Sludge and Industrial Wastewater Biogas-Producing Systems journal May 2016
Characterization of Chemosynthetic Microbial Mats Associated with Intertidal Hydrothermal Sulfur Vents in White Point, San Pedro, CA, USA journal July 2016
Seasonal Succession and Spatial Patterns of Synechococcus Microdiversity in a Salt Marsh Estuary Revealed through 16S rRNA Gene Oligotyping journal August 2017
Uncultured Gammaproteobacteria and Desulfobacteraceae Account for Major Acetate Assimilation in a Coastal Marine Sediment journal December 2018
An ensemble approach to the structure-function problem in microbial communities text January 2021
Hard and soft plastic resin embedding for single-cell element uptake investigations of marine-snow-associated microorganisms using nano-scale secondary ion mass spectrometry: NanoSIMS of sectioned marine snow samples journal July 2018
Intracellular calcite and sulfur dynamics of Achromatium cells observed in a lab-based enrichment and aerobic incubation experiment journal September 2018
Oxygen loss from seagrass roots coincides with colonisation of sulphide-oxidising cable bacteria and reduces sulphide stress journal October 2018
Understanding how microbiomes influence the systems they inhabit journal August 2018
Heavy water and 15 N labelling with NanoSIMS analysis reveals growth rate-dependent metabolic heterogeneity in chemostats : NanoSIMS analysis of metabolic diversity in chemostats journal March 2015
Environmental insights from high-resolution (SIMS) sulfur isotope analyses of sulfides in Proterozoic microbialites with diverse mat textures journal October 2017
Secondary Ion Mass Spectrometry Methodology for Isotopic Ratio Measurement of Micro‐Grains in Thin Sections: True Grain Size Estimation and Deconvolution of Inter‐Grain Size Gradients and Intra‐Grain Radial Gradients journal December 2018
A conceptual framework for the phylogenetically constrained assembly of microbial communities journal October 2019
Shotgun Metagenomics Reveals the Benthic Microbial Community Response to Plastic and Bioplastic in a Coastal Marine Environment journal June 2019

Similar Records

The Green Berry Consortia of the Sippewissett Salt Marsh: Millimeter-Sized Aggregates of Diazotrophic Unicellular Cyanobacteria
Journal Article · Mon Sep 04 00:00:00 EDT 2017 · Frontiers in Microbiology · OSTI ID:1468986
Active sulfur cycling in the terrestrial deep subsurface
Journal Article · Mon Feb 10 23:00:00 EST 2020 · The ISME Journal · OSTI ID:1606636

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Microbiology