Microscale sulfur cycling in the phototrophic pink berry consortia of the Sippewissett Salt Marsh: Sulfur cycling in pink berries of the Sippewissett Marsh
Abstract
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 andmore »
- Authors:
-
- Univ. of California, Davis, CA (United States). Dept. of Microbiology Graduate Group
- Shell Technology Norway, Oslo (Norway). Arctic Technology; Harvard Univ., Cambridge, MA (United States). Dept. of Organismic and Evolutionary Biology
- Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Marine Sciences
- Univ. of Arizona, Tucson, AZ (United States). Ecology and Evolutionary Biology
- 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
- Univ. of California, Davis, CA (United States). UC Davis Genome Center; Univ. of California, Davis, CA (United States). Dept. of Biomedical Engineering
- Cornell Univ., Ithaca, NY (United States). Crop and Soil Sciences
- Cornell Univ., Ithaca, NY (United States). Dept. of Microbiology
- Indiana Univ.--Purdue Univ., Indianapolis, IN (United States). Dept. of Earth Sciences
- Washington University, St. Louis, MO (United States). Dept. of Earth and Planetary Sciences
- California Institute of Technology (CalTech), Pasadena, CA (United States). Division of Geological and Planetary Sciences
- Publication Date:
- Research Org.:
- Marine Biological Laboratory, Woods Hole, MA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
- OSTI Identifier:
- 1625847
- Grant/Contract Number:
- FG02-85ER13361
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Environmental Microbiology
- Additional Journal Information:
- Journal Volume: 16; Journal Issue: 11; Journal ID: ISSN 1462-2912
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Microbiology
Citation Formats
Wilbanks, Elizabeth G., Jaekel, Ulrike, Salman, Verena, Humphrey, Parris T., Eisen, Jonathan A., Facciotti, Marc T., Buckley, Daniel H., Zinder, Stephen H., Druschel, Gregory K., Fike, David A., and Orphan, Victoria J. Microscale sulfur cycling in the phototrophic pink berry consortia of the Sippewissett Salt Marsh: Sulfur cycling in pink berries of the Sippewissett Marsh. United States: N. p., 2014.
Web. doi:10.1111/1462-2920.12388.
Wilbanks, Elizabeth G., Jaekel, Ulrike, Salman, Verena, Humphrey, Parris T., Eisen, Jonathan A., Facciotti, Marc T., Buckley, Daniel H., Zinder, Stephen H., Druschel, Gregory K., Fike, David A., & Orphan, Victoria J. Microscale sulfur cycling in the phototrophic pink berry consortia of the Sippewissett Salt Marsh: Sulfur cycling in pink berries of the Sippewissett Marsh. United States. https://doi.org/10.1111/1462-2920.12388
Wilbanks, Elizabeth G., Jaekel, Ulrike, Salman, Verena, Humphrey, Parris T., Eisen, Jonathan A., Facciotti, Marc T., Buckley, Daniel H., Zinder, Stephen H., Druschel, Gregory K., Fike, David A., and Orphan, Victoria J. Wed .
"Microscale sulfur cycling in the phototrophic pink berry consortia of the Sippewissett Salt Marsh: Sulfur cycling in pink berries of the Sippewissett Marsh". United States. https://doi.org/10.1111/1462-2920.12388. https://www.osti.gov/servlets/purl/1625847.
@article{osti_1625847,
title = {Microscale sulfur cycling in the phototrophic pink berry consortia of the Sippewissett Salt Marsh: Sulfur cycling in pink berries of the Sippewissett Marsh},
author = {Wilbanks, Elizabeth G. and Jaekel, Ulrike and Salman, Verena and Humphrey, Parris T. and Eisen, Jonathan A. and Facciotti, Marc T. and Buckley, Daniel H. and Zinder, Stephen H. and Druschel, Gregory K. and Fike, David A. and Orphan, Victoria J.},
abstractNote = {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.},
doi = {10.1111/1462-2920.12388},
journal = {Environmental Microbiology},
number = 11,
volume = 16,
place = {United States},
year = {Wed Feb 26 00:00:00 EST 2014},
month = {Wed Feb 26 00:00:00 EST 2014}
}
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