Functional gene diversity of oolitic sands from Great Bahama Bank
Despite the importance of oolitic depositional systems as indicators of climate and reservoirs of inorganic C, little is known about the microbial functional diversity, structure, composition, and potential metabolic processes leading to precipitation of carbonates. To fill this gap, we assess the m...
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Published in | Geobiology Vol. 12; no. 3; pp. 231 - 249 |
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Format | Journal Article |
Language | English |
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Blackwell Publishing Ltd
01.05.2014
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Abstract | Despite the importance of oolitic depositional systems as indicators of climate and reservoirs of inorganic C, little is known about the microbial functional diversity, structure, composition, and potential metabolic processes leading to precipitation of carbonates. To fill this gap, we assess the metabolic gene carriage and extracellular polymeric substance (EPS) development in microbial communities associated with oolitic carbonate sediments from the Bahamas Archipelago. Oolitic sediments ranging from high‐energy ‘active’ to lower energy ‘non‐active’ and ‘microbially stabilized’ environments were examined as they represent contrasting depositional settings, mostly influenced by tidal flows and wave‐generated currents. Functional gene analysis, which employed a microarray‐based gene technology, detected a total of 12 432 of 95 847 distinct gene probes, including a large number of metabolic processes previously linked to mineral precipitation. Among these, gene‐encoding enzymes for denitrification, sulfate reduction, ammonification, and oxygenic/anoxygenic photosynthesis were abundant. In addition, a broad diversity of genes was related to organic carbon degradation, and N2 fixation implying these communities has metabolic plasticity that enables survival under oligotrophic conditions. Differences in functional genes were detected among the environments, with higher diversity associated with non‐active and microbially stabilized environments in comparison with the active environment. EPS showed a gradient increase from active to microbially stabilized communities, and when combined with functional gene analysis, which revealed genes encoding EPS‐degrading enzymes (chitinases, glucoamylase, amylases), supports a putative role of EPS‐mediated microbial calcium carbonate precipitation. We propose that carbonate precipitation in marine oolitic biofilms is spatially and temporally controlled by a complex consortium of microbes with diverse physiologies, including photosynthesizers, heterotrophs, denitrifiers, sulfate reducers, and ammonifiers. |
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AbstractList | Abstract
Despite the importance of oolitic depositional systems as indicators of climate and reservoirs of inorganic C, little is known about the microbial functional diversity, structure, composition, and potential metabolic processes leading to precipitation of carbonates. To fill this gap, we assess the metabolic gene carriage and extracellular polymeric substance (
EPS
) development in microbial communities associated with oolitic carbonate sediments from the Bahamas Archipelago. Oolitic sediments ranging from high‐energy ‘active’ to lower energy ‘non‐active’ and ‘microbially stabilized’ environments were examined as they represent contrasting depositional settings, mostly influenced by tidal flows and wave‐generated currents. Functional gene analysis, which employed a microarray‐based gene technology, detected a total of 12 432 of 95 847 distinct gene probes, including a large number of metabolic processes previously linked to mineral precipitation. Among these, gene‐encoding enzymes for denitrification, sulfate reduction, ammonification, and oxygenic/anoxygenic photosynthesis were abundant. In addition, a broad diversity of genes was related to organic carbon degradation, and N
2
fixation implying these communities has metabolic plasticity that enables survival under oligotrophic conditions. Differences in functional genes were detected among the environments, with higher diversity associated with non‐active and microbially stabilized environments in comparison with the active environment.
EPS
showed a gradient increase from active to microbially stabilized communities, and when combined with functional gene analysis, which revealed genes encoding
EPS
‐degrading enzymes (chitinases, glucoamylase, amylases), supports a putative role of
EPS
‐mediated microbial calcium carbonate precipitation. We propose that carbonate precipitation in marine oolitic biofilms is spatially and temporally controlled by a complex consortium of microbes with diverse physiologies, including photosynthesizers, heterotrophs, denitrifiers, sulfate reducers, and ammonifiers. Despite the importance of oolitic depositional systems as indicators of climate and reservoirs of inorganic C, little is known about the microbial functional diversity, structure, composition, and potential metabolic processes leading to precipitation of carbonates. To fill this gap, we assess the metabolic gene carriage and extracellular polymeric substance (EPS) development in microbial communities associated with oolitic carbonate sediments from the Bahamas Archipelago. Oolitic sediments ranging from high‐energy ‘active’ to lower energy ‘non‐active’ and ‘microbially stabilized’ environments were examined as they represent contrasting depositional settings, mostly influenced by tidal flows and wave‐generated currents. Functional gene analysis, which employed a microarray‐based gene technology, detected a total of 12 432 of 95 847 distinct gene probes, including a large number of metabolic processes previously linked to mineral precipitation. Among these, gene‐encoding enzymes for denitrification, sulfate reduction, ammonification, and oxygenic/anoxygenic photosynthesis were abundant. In addition, a broad diversity of genes was related to organic carbon degradation, and N2 fixation implying these communities has metabolic plasticity that enables survival under oligotrophic conditions. Differences in functional genes were detected among the environments, with higher diversity associated with non‐active and microbially stabilized environments in comparison with the active environment. EPS showed a gradient increase from active to microbially stabilized communities, and when combined with functional gene analysis, which revealed genes encoding EPS‐degrading enzymes (chitinases, glucoamylase, amylases), supports a putative role of EPS‐mediated microbial calcium carbonate precipitation. We propose that carbonate precipitation in marine oolitic biofilms is spatially and temporally controlled by a complex consortium of microbes with diverse physiologies, including photosynthesizers, heterotrophs, denitrifiers, sulfate reducers, and ammonifiers. Despite the importance of oolitic depositional systems as indicators of climate and reservoirs of inorganic C, little is known about the microbial functional diversity, structure, composition, and potential metabolic processes leading to precipitation of carbonates. To fill this gap, we assess the metabolic gene carriage and extracellular polymeric substance (EPS) development in microbial communities associated with oolitic carbonate sediments from the Bahamas Archipelago. Oolitic sediments ranging from high-energy 'active' to lower energy 'non-active' and 'microbially stabilized' environments were examined as they represent contrasting depositional settings, mostly influenced by tidal flows and wave-generated currents. Functional gene analysis, which employed a microarray-based gene technology, detected a total of 12 432 of 95 847 distinct gene probes, including a large number of metabolic processes previously linked to mineral precipitation. Among these, gene-encoding enzymes for denitrification, sulfate reduction, ammonification, and oxygenic/anoxygenic photosynthesis were abundant. In addition, a broad diversity of genes was related to organic carbon degradation, and N2 fixation implying these communities has metabolic plasticity that enables survival under oligotrophic conditions. Differences in functional genes were detected among the environments, with higher diversity associated with non-active and microbially stabilized environments in comparison with the active environment. EPS showed a gradient increase from active to microbially stabilized communities, and when combined with functional gene analysis, which revealed genes encoding EPS-degrading enzymes (chitinases, glucoamylase, amylases), supports a putative role of EPS-mediated microbial calcium carbonate precipitation. We propose that carbonate precipitation in marine oolitic biofilms is spatially and temporally controlled by a complex consortium of microbes with diverse physiologies, including photosynthesizers, heterotrophs, denitrifiers, sulfate reducers, and ammonifiers. |
Author | Piggot, A. M. Van Norstrand, J. D. Eberli, G. P. Klaus, J. S. Diaz, M. R. Zhou, J. |
Author_xml | – sequence: 1 givenname: M. R. surname: Diaz fullname: Diaz, M. R. email: mdiaz@rsmas.miami.edu organization: Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Science, University of Miami, FL, Miami, USA – sequence: 2 givenname: J. D. surname: Van Norstrand fullname: Van Norstrand, J. D. organization: Department of Microbiology and Plant Biology, Institute for Environmental Genomics, University of Oklahoma, OK, Norman, USA – sequence: 3 givenname: G. P. surname: Eberli fullname: Eberli, G. P. organization: Marine Geology and Geophysics, Rosenstiel School of Marine and Atmospheric Science, University of Miami, FL, Miami, USA – sequence: 4 givenname: A. M. surname: Piggot fullname: Piggot, A. M. organization: Marine Geology and Geophysics, Rosenstiel School of Marine and Atmospheric Science, University of Miami, FL, Miami, USA – sequence: 5 givenname: J. surname: Zhou fullname: Zhou, J. organization: Department of Microbiology and Plant Biology, Institute for Environmental Genomics, University of Oklahoma, OK, Norman, USA – sequence: 6 givenname: J. S. surname: Klaus fullname: Klaus, J. S. organization: Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, FL, USA |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24612324$$D View this record in MEDLINE/PubMed |
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Copyright | 2014 John Wiley & Sons Ltd 2014 John Wiley & Sons Ltd. Copyright © 2014 John Wiley & Sons Ltd |
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Notes | ArticleID:GBI12079 ark:/67375/WNG-3MZN6RJS-J istex:EEC615FCC87F078C3E8CEEBBA79EF8A51EFD09A2 Industrial Associates of the University of Miami Center for Carbonate Research (CSL) Fig. S1 Relative abundance of phylogenetic groups associated with autotrophic carbon fixation. (A) pcc/acc (propionyl-CoA/acetyl-CoA carboxylase); (B) RuBisCO ribulose (1,5-biphosphate carboxylase/oxygenase); (C) carbon monoxide dehydrogenase (CODH); (D) aclB-ATP (ATP citrate lyase). Relative abundance is based on the total signal intensities of all genes associated with each particular carbon fixation pathway. Proteobacteria phylum is divided into the classes, Alpha-, Beta-, Gamma-, Epsilon-.Fig. S2 Phylogenetic distribution and normalized signal intensity of genes associated with representative microbial genera associated with acetogenesis and methanotrophy. (A) Representative distribution of acetogens at phylum level. Proteobacteria phylum is divided into the classes, Alpha- and Gamma-; (B) Distribution of acetogens at genus level. Proteobacteria phylum is divided into the classes, Alpha-, Beta-, Gamma-; (C) Distribution of methanotrophs at phylum level; and (D) Distribution of methanotrophs at genus level. Relative abundance is based on the total signal intensities of genes associated with each particular geochemical cycle.Fig. S3 Phylogenetic distribution of genes associated with denitrification. (A) Representative distribution of denitrifiers at phylum level. Proteobacteria phylum is divided into the classes, Alpha-, Beta-, Gamma-; (B) Distribution of denitrifiers at genus level. Relative abundance is based on the total signal intensities of all denitrification genes within a given phylogenetic group.Fig. S4 Phylogenetic distribution of genes involved in ammonification. Relative abundance is based on the total signal intensities of all genes associated with ammonification. Proteobacteria phylum is divided into the classes, Alpha-, Beta-, Delta-, Gamma-.Fig. S5 Phylogenetic distribution of genes associated with N2 fixation. (A) Representative distribution of N2- fixers at phylum level. Proteobacteria phylum is divided into the classes, Alpha-, Beta-, Delta-, Epsilon-. (B) Distribution of N2 fixers at genus level. Relative abundance is based on the total signal intensities of N2 fixation genes within a given phylogenetic group.Fig. S6 Phylogenetic distribution of genes associated with sulfate reduction. (A) Representative distribution of sulfate reducers at phylum level. Proteobacteria phylum is divided into the classes, Alpha-, Beta-, Delta-, Gamma-. (B) Distribution of sulfate reducers at genus level. Relative abundance is based on the total signal intensities of sulfate-reducing genes within a given phylogenetic group.Table S1 Summary of geochip 4.2 probes and covered gene sequences among different categories. ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
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SubjectTerms | Archaea - genetics Archaea - metabolism Bacteria - genetics Bacteria - metabolism Bahamas Carbon Cycle Carbonates - metabolism Fungi - genetics Fungi - metabolism Genetic Variation Geologic Sediments - microbiology Nitrogen Cycle Polymerase Chain Reaction Sulfur - metabolism |
Title | Functional gene diversity of oolitic sands from Great Bahama Bank |
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