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Impact of Seasonal Hypoxia on Activity and Community Structure of Chemolithoautotrophic Bacteria in a Coastal Sediment.
Appl Environ Microbiol. 2017 05 15; 83(10)AE

Abstract

Seasonal hypoxia in coastal systems drastically changes the availability of electron acceptors in bottom water, which alters the sedimentary reoxidation of reduced compounds. However, the effect of seasonal hypoxia on the chemolithoautotrophic community that catalyzes these reoxidation reactions is rarely studied. Here, we examine the changes in activity and structure of the sedimentary chemolithoautotrophic bacterial community of a seasonally hypoxic saline basin under oxic (spring) and hypoxic (summer) conditions. Combined 16S rRNA gene amplicon sequencing and analysis of phospholipid-derived fatty acids indicated a major temporal shift in community structure. Aerobic sulfur-oxidizing Gammaproteobacteria (Thiotrichales) and Epsilonproteobacteria (Campylobacterales) were prevalent during spring, whereas Deltaproteobacteria (Desulfobacterales) related to sulfate-reducing bacteria prevailed during summer hypoxia. Chemolithoautotrophy rates in the surface sediment were three times higher in spring than in summer. The depth distribution of chemolithoautotrophy was linked to the distinct sulfur oxidation mechanisms identified through microsensor profiling, i.e., canonical sulfur oxidation, electrogenic sulfur oxidation by cable bacteria, and sulfide oxidation coupled to nitrate reduction by Beggiatoaceae The metabolic diversity of the sulfur-oxidizing bacterial community suggests a complex niche partitioning within the sediment, probably driven by the availability of reduced sulfur compounds (H2S, S0, and S2O32-) and electron acceptors (O2 and NO3-) regulated by seasonal hypoxia.IMPORTANCE Chemolithoautotrophic microbes in the seafloor are dependent on electron acceptors, like oxygen and nitrate, that diffuse from the overlying water. Seasonal hypoxia, however, drastically changes the availability of these electron acceptors in the bottom water; hence, one expects a strong impact of seasonal hypoxia on sedimentary chemolithoautotrophy. A multidisciplinary investigation of the sediments in a seasonally hypoxic coastal basin confirms this hypothesis. Our data show that bacterial community structure and chemolithoautotrophic activity varied with the seasonal depletion of oxygen. Unexpectedly, the dark carbon fixation was also dependent on the dominant microbial pathway of sulfur oxidation occurring in the sediment (i.e., canonical sulfur oxidation, electrogenic sulfur oxidation by cable bacteria, and sulfide oxidation coupled to nitrate reduction by Beggiatoaceae). These results suggest that a complex niche partitioning within the sulfur-oxidizing bacterial community additionally affects the chemolithoautotrophic community of seasonally hypoxic sediments.

Authors+Show Affiliations

Department of Marine Microbiology and Biogeochemistry and Department of Estuarine and Delta Systems, NIOZ Royal Netherlands Institute for Sea Research, Texel and Yerseke, and Utrecht University, Utrecht, The Netherlands.Department of Marine Microbiology and Biogeochemistry and Department of Estuarine and Delta Systems, NIOZ Royal Netherlands Institute for Sea Research, Texel and Yerseke, and Utrecht University, Utrecht, The Netherlands.Department of Marine Microbiology and Biogeochemistry and Department of Estuarine and Delta Systems, NIOZ Royal Netherlands Institute for Sea Research, Texel and Yerseke, and Utrecht University, Utrecht, The Netherlands.Section for Microbiology, Department of Bioscience, Aarhus University, Aarhus, Denmark.Department of Marine Microbiology and Biogeochemistry and Department of Estuarine and Delta Systems, NIOZ Royal Netherlands Institute for Sea Research, Texel and Yerseke, and Utrecht University, Utrecht, The Netherlands.Department of Marine Microbiology and Biogeochemistry and Department of Estuarine and Delta Systems, NIOZ Royal Netherlands Institute for Sea Research, Texel and Yerseke, and Utrecht University, Utrecht, The Netherlands. Faculty of Geosciences, Department of Earth Sciences, Utrecht University, Utrecht, The Netherlands.Department of Marine Microbiology and Biogeochemistry and Department of Estuarine and Delta Systems, NIOZ Royal Netherlands Institute for Sea Research, Texel and Yerseke, and Utrecht University, Utrecht, The Netherlands. Section for Microbiology, Department of Bioscience, Aarhus University, Aarhus, Denmark. Department of Environmental, Analytical, and Geo-Chemistry, Vrije Universiteit Brussel (VUB), Brussels, Belgium.Department of Marine Microbiology and Biogeochemistry and Department of Estuarine and Delta Systems, NIOZ Royal Netherlands Institute for Sea Research, Texel and Yerseke, and Utrecht University, Utrecht, The Netherlands laura.villanueva@nioz.nl eric.boschker@nioz.nl.Department of Marine Microbiology and Biogeochemistry and Department of Estuarine and Delta Systems, NIOZ Royal Netherlands Institute for Sea Research, Texel and Yerseke, and Utrecht University, Utrecht, The Netherlands laura.villanueva@nioz.nl eric.boschker@nioz.nl. Section for Microbiology, Department of Bioscience, Aarhus University, Aarhus, Denmark.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

28314724

Citation

Lipsewers, Yvonne A., et al. "Impact of Seasonal Hypoxia On Activity and Community Structure of Chemolithoautotrophic Bacteria in a Coastal Sediment." Applied and Environmental Microbiology, vol. 83, no. 10, 2017.
Lipsewers YA, Vasquez-Cardenas D, Seitaj D, et al. Impact of Seasonal Hypoxia on Activity and Community Structure of Chemolithoautotrophic Bacteria in a Coastal Sediment. Appl Environ Microbiol. 2017;83(10).
Lipsewers, Y. A., Vasquez-Cardenas, D., Seitaj, D., Schauer, R., Hidalgo-Martinez, S., Sinninghe Damsté, J. S., Meysman, F. J. R., Villanueva, L., & Boschker, H. T. S. (2017). Impact of Seasonal Hypoxia on Activity and Community Structure of Chemolithoautotrophic Bacteria in a Coastal Sediment. Applied and Environmental Microbiology, 83(10). https://doi.org/10.1128/AEM.03517-16
Lipsewers YA, et al. Impact of Seasonal Hypoxia On Activity and Community Structure of Chemolithoautotrophic Bacteria in a Coastal Sediment. Appl Environ Microbiol. 2017 05 15;83(10) PubMed PMID: 28314724.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Impact of Seasonal Hypoxia on Activity and Community Structure of Chemolithoautotrophic Bacteria in a Coastal Sediment. AU - Lipsewers,Yvonne A, AU - Vasquez-Cardenas,Diana, AU - Seitaj,Dorina, AU - Schauer,Regina, AU - Hidalgo-Martinez,Silvia, AU - Sinninghe Damsté,Jaap S, AU - Meysman,Filip J R, AU - Villanueva,Laura, AU - Boschker,Henricus T S, Y1 - 2017/05/01/ PY - 2016/12/30/received PY - 2017/03/09/accepted PY - 2017/3/21/pubmed PY - 2017/11/29/medline PY - 2017/3/19/entrez KW - Beggiatoaceae KW - CCB cycle KW - cable bacteria KW - chemoautotrophy KW - dark carbon fixation KW - phospholipid-derived fatty acid (PLFA) KW - rTCA cycle KW - stable isotope probing (SIP) KW - sulfur oxidation JF - Applied and environmental microbiology JO - Appl Environ Microbiol VL - 83 IS - 10 N2 - Seasonal hypoxia in coastal systems drastically changes the availability of electron acceptors in bottom water, which alters the sedimentary reoxidation of reduced compounds. However, the effect of seasonal hypoxia on the chemolithoautotrophic community that catalyzes these reoxidation reactions is rarely studied. Here, we examine the changes in activity and structure of the sedimentary chemolithoautotrophic bacterial community of a seasonally hypoxic saline basin under oxic (spring) and hypoxic (summer) conditions. Combined 16S rRNA gene amplicon sequencing and analysis of phospholipid-derived fatty acids indicated a major temporal shift in community structure. Aerobic sulfur-oxidizing Gammaproteobacteria (Thiotrichales) and Epsilonproteobacteria (Campylobacterales) were prevalent during spring, whereas Deltaproteobacteria (Desulfobacterales) related to sulfate-reducing bacteria prevailed during summer hypoxia. Chemolithoautotrophy rates in the surface sediment were three times higher in spring than in summer. The depth distribution of chemolithoautotrophy was linked to the distinct sulfur oxidation mechanisms identified through microsensor profiling, i.e., canonical sulfur oxidation, electrogenic sulfur oxidation by cable bacteria, and sulfide oxidation coupled to nitrate reduction by Beggiatoaceae The metabolic diversity of the sulfur-oxidizing bacterial community suggests a complex niche partitioning within the sediment, probably driven by the availability of reduced sulfur compounds (H2S, S0, and S2O32-) and electron acceptors (O2 and NO3-) regulated by seasonal hypoxia.IMPORTANCE Chemolithoautotrophic microbes in the seafloor are dependent on electron acceptors, like oxygen and nitrate, that diffuse from the overlying water. Seasonal hypoxia, however, drastically changes the availability of these electron acceptors in the bottom water; hence, one expects a strong impact of seasonal hypoxia on sedimentary chemolithoautotrophy. A multidisciplinary investigation of the sediments in a seasonally hypoxic coastal basin confirms this hypothesis. Our data show that bacterial community structure and chemolithoautotrophic activity varied with the seasonal depletion of oxygen. Unexpectedly, the dark carbon fixation was also dependent on the dominant microbial pathway of sulfur oxidation occurring in the sediment (i.e., canonical sulfur oxidation, electrogenic sulfur oxidation by cable bacteria, and sulfide oxidation coupled to nitrate reduction by Beggiatoaceae). These results suggest that a complex niche partitioning within the sulfur-oxidizing bacterial community additionally affects the chemolithoautotrophic community of seasonally hypoxic sediments. SN - 1098-5336 UR - https://www.unboundmedicine.com/medline/citation/28314724/Impact_of_Seasonal_Hypoxia_on_Activity_and_Community_Structure_of_Chemolithoautotrophic_Bacteria_in_a_Coastal_Sediment_ L2 - http://aem.asm.org/cgi/pmidlookup?view=long&pmid=28314724 DB - PRIME DP - Unbound Medicine ER -