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

被引:73
作者
Wilbanks, Elizabeth G. [1 ]
Jaekel, Ulrike [6 ,7 ]
Salman, Verena [8 ]
Humphrey, Parris T. [9 ]
Eisen, Jonathan A. [2 ,3 ,5 ]
Facciotti, Marc T. [4 ,5 ]
Buckley, Daniel H. [10 ]
Zinder, Stephen H. [11 ]
Druschel, Gregory K. [12 ]
Fike, David A. [13 ]
Orphan, Victoria J. [14 ]
机构
[1] Univ Calif Davis, Dept Microbiol Grad Grp, Davis, CA 95616 USA
[2] Univ Calif Davis, Dept Evolut & Ecol, Davis, CA 95616 USA
[3] Univ Calif Davis, Dept Microbiol & Immunol, Davis, CA 95616 USA
[4] Univ Calif Davis, Dept Biomed Engn, Davis, CA 95616 USA
[5] Univ Calif Davis, UC Davis Genome Ctr, Davis, CA 95616 USA
[6] Shell Technol Norway, Arctic Technol, N-0277 Oslo, Norway
[7] Harvard Univ, Dept Organism & Evolutionary Biol, Cambridge, MA 02138 USA
[8] Univ N Carolina, Dept Marine Sci, Chapel Hill, NC 27599 USA
[9] Univ Arizona, Tucson, AZ 85721 USA
[10] Cornell Univ, Ithaca, NY 14853 USA
[11] Cornell Univ, Dept Microbiol, Ithaca, NY 14853 USA
[12] Indiana Univ Purdue Univ, Dept Earth Sci, Indianapolis, IN 46202 USA
[13] Washington Univ, Dept Earth & Planetary Sci, St Louis, MO 63130 USA
[14] CALTECH, Div Geol & Planetary Sci, Pasadena, CA 91125 USA
基金
美国国家科学基金会;
关键词
IN-SITU HYBRIDIZATION; TARGETED OLIGONUCLEOTIDE PROBES; SULFATE-REDUCING BACTERIA; ISOTOPE FRACTIONATION; ANAEROBIC OXIDATION; MAXIMUM-LIKELIHOOD; ELEMENTAL SULFUR; MICROBIAL MATS; DESULFOCAPSA-SULFOEXIGENS; PHOTOSYNTHETIC BACTERIUM;
D O I
10.1111/1462-2920.12388
中图分类号
Q93 [微生物学];
学科分类号
071005 ; 100705 ;
摘要
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 S-34-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 0-500m. Sulfide within the berries, captured on silver wires and analysed using secondary ion mass spectrometer, increased in abundance towards the berry interior, while S-34-(sulfide) decreased from 6 parts per thousand to -31 parts per thousand from the exterior to interior of the berry. These values correspond to sulfate-sulfide isotopic fractionations (15-53 parts per thousand) 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.
引用
收藏
页码:3398 / 3415
页数:18
相关论文
共 93 条
[1]   Resistance, resilience, and redundancy in microbial communities [J].
Allison, Steven D. ;
Martiny, Jennifer B. H. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2008, 105 :11512-11519
[2]   COMBINATION OF 16S RIBOSOMAL-RNA-TARGETED OLIGONUCLEOTIDE PROBES WITH FLOW-CYTOMETRY FOR ANALYZING MIXED MICROBIAL-POPULATIONS [J].
AMANN, RI ;
BINDER, BJ ;
OLSON, RJ ;
CHISHOLM, SW ;
DEVEREUX, R ;
STAHL, DA .
APPLIED AND ENVIRONMENTAL MICROBIOLOGY, 1990, 56 (06) :1919-1925
[3]   Microbial Species Richness and Metabolic Activities in Hypersaline Microbial Mats: Insight into Biosignature Formation Through Lithification [J].
Baumgartner, Laura K. ;
Dupraz, Christophe ;
Buckley, Daniel H. ;
Spear, John R. ;
Pace, Norman R. ;
Visscher, Pieter T. .
ASTROBIOLOGY, 2009, 9 (09) :861-874
[4]   Sulfate reducing bacteria in microbial mats: Changing paradigms, new discoveries [J].
Baumgartner, LK ;
Reid, RP ;
Dupraz, C ;
Decho, AW ;
Buckley, DH ;
Spear, JR ;
Przekop, KM ;
Visscher, PT .
SEDIMENTARY GEOLOGY, 2006, 185 (3-4) :131-145
[5]   A marine microbial consortium apparently mediating anaerobic oxidation of methane [J].
Boetius, A ;
Ravenschlag, K ;
Schubert, CJ ;
Rickert, D ;
Widdel, F ;
Gieseke, A ;
Amann, R ;
Jorgensen, BB ;
Witte, U ;
Pfannkuche, O .
NATURE, 2000, 407 (6804) :623-626
[6]   DEVELOPMENT OF A GOLD AMALGAM VOLTAMMETRIC MICROELECTRODE FOR THE DETERMINATION OF DISSOLVED FE, MN, O-2, AND S(-II) IN POREWATERS OF MARINE AND FRESH-WATER SEDIMENTS [J].
BRENDEL, PJ ;
LUTHER, GW .
ENVIRONMENTAL SCIENCE & TECHNOLOGY, 1995, 29 (03) :751-761
[7]  
Bruchert V., 2004, SPECIAL PAPER 379 SU, P1, DOI [10.1130/0-8137-2379-5.1, DOI 10.1130/0-8137-2379-5.1, 10.1130/0-8137-2379-5.1.]
[8]   Anoxic carbon flux in photosynthetic microbial mats as revealed by metatranscriptomics [J].
Burow, Luke C. ;
Woebken, Dagmar ;
Marshall, Ian P. G. ;
Lindquist, Erika A. ;
Bebout, Brad M. ;
Prufert-Bebout, Leslie ;
Hoehler, Tori M. ;
Tringe, Susannah G. ;
Pett-Ridge, Jennifer ;
Weber, Peter K. ;
Spormann, Alfred M. ;
Singer, Steven W. .
ISME JOURNAL, 2013, 7 (04) :817-829
[9]   BIOGEOCHEMICAL CYCLES OF CARBON, SULFUR, AND FREE OXYGEN IN A MICROBIAL MAT [J].
CANFIELD, DE ;
MARAIS, DJD .
GEOCHIMICA ET COSMOCHIMICA ACTA, 1993, 57 (16) :3971-3984
[10]   Biogeochemistry of sulfur isotopes [J].
Canfield, DE .
STABLE ISOTOPE GEOCHEMISTRY, 2001, 43 :607-636