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Increased Denitrification Rates Associated with Shifts in Prokaryotic Community Composition Caused by Varying Hydrologic Connectivity

While modern developments in agriculture have allowed for increases in crop yields and rapid human population growth, they have also drastically altered biogeochemical cycles, including the biotransformation of nitrogen. Denitrification is a critical process performed by bacteria and fungi that remo...

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Autores principales: Tomasek, Abigail, Staley, Christopher, Wang, Ping, Kaiser, Thomas, Lurndahl, Nicole, Kozarek, Jessica L., Hondzo, Miki, Sadowsky, Michael J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5702768/
https://www.ncbi.nlm.nih.gov/pubmed/29213260
http://dx.doi.org/10.3389/fmicb.2017.02304
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author Tomasek, Abigail
Staley, Christopher
Wang, Ping
Kaiser, Thomas
Lurndahl, Nicole
Kozarek, Jessica L.
Hondzo, Miki
Sadowsky, Michael J.
author_facet Tomasek, Abigail
Staley, Christopher
Wang, Ping
Kaiser, Thomas
Lurndahl, Nicole
Kozarek, Jessica L.
Hondzo, Miki
Sadowsky, Michael J.
author_sort Tomasek, Abigail
collection PubMed
description While modern developments in agriculture have allowed for increases in crop yields and rapid human population growth, they have also drastically altered biogeochemical cycles, including the biotransformation of nitrogen. Denitrification is a critical process performed by bacteria and fungi that removes nitrate in surface waters, thereby serving as a potential natural remediation strategy. We previously reported that constant inundation resulted in a coupling of denitrification gene abundances with denitrification rates in sediments, but these relationships were not maintained in periodically-inundated or non-inundated environments. In this study, we utilized Illumina next-generation sequencing to further evaluate how the microbial community responds to these hydrologic regimes and how this community is related to denitrification rates at three sites along a creek in an agricultural watershed over 2 years. The hydrologic connectivity of the sampling location had a significantly greater influence on the denitrification rate (P = 0.010), denitrification gene abundances (P < 0.001), and the prokaryotic community (P < 0.001), than did other spatiotemporal factors (e.g., creek sample site or sample month) within the same year. However, annual variability among denitrification rates was also observed (P < 0.001). Furthermore, the denitrification rate was significantly positively correlated with water nitrate concentration (Spearman's ρ = 0.56, P < 0.0001), denitrification gene abundances (ρ = 0.23–0.47, P ≤ 0.006), and the abundances of members of the families Burkholderiaceae, Anaerolinaceae, Microbacteriaceae, Acidimicrobineae incertae sedis, Cytophagaceae, and Hyphomicrobiaceae (ρ = 0.17–0.25, P ≤ 0.041). Prokaryotic community composition accounted for the least amount of variation in denitrification rates (22%), while the collective influence of spatiotemporal factors and gene abundances accounted for 37%, with 40% of the variation related to interactions among all parameters. Results of this study suggest that the hydrologic connectivity at each location had a greater effect on the prokaryotic community than did spatiotemporal differences, where inundation is associated with shifts favoring increased denitrification potential. We further establish that while complex interactions among the prokaryotic community influence denitrification, the link between hydrologic connectivity, microbial community composition, and genetic potential for biogeochemical cycling is a promising avenue to explore hydrologic remediation strategies such as periodic flooding.
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spelling pubmed-57027682017-12-06 Increased Denitrification Rates Associated with Shifts in Prokaryotic Community Composition Caused by Varying Hydrologic Connectivity Tomasek, Abigail Staley, Christopher Wang, Ping Kaiser, Thomas Lurndahl, Nicole Kozarek, Jessica L. Hondzo, Miki Sadowsky, Michael J. Front Microbiol Microbiology While modern developments in agriculture have allowed for increases in crop yields and rapid human population growth, they have also drastically altered biogeochemical cycles, including the biotransformation of nitrogen. Denitrification is a critical process performed by bacteria and fungi that removes nitrate in surface waters, thereby serving as a potential natural remediation strategy. We previously reported that constant inundation resulted in a coupling of denitrification gene abundances with denitrification rates in sediments, but these relationships were not maintained in periodically-inundated or non-inundated environments. In this study, we utilized Illumina next-generation sequencing to further evaluate how the microbial community responds to these hydrologic regimes and how this community is related to denitrification rates at three sites along a creek in an agricultural watershed over 2 years. The hydrologic connectivity of the sampling location had a significantly greater influence on the denitrification rate (P = 0.010), denitrification gene abundances (P < 0.001), and the prokaryotic community (P < 0.001), than did other spatiotemporal factors (e.g., creek sample site or sample month) within the same year. However, annual variability among denitrification rates was also observed (P < 0.001). Furthermore, the denitrification rate was significantly positively correlated with water nitrate concentration (Spearman's ρ = 0.56, P < 0.0001), denitrification gene abundances (ρ = 0.23–0.47, P ≤ 0.006), and the abundances of members of the families Burkholderiaceae, Anaerolinaceae, Microbacteriaceae, Acidimicrobineae incertae sedis, Cytophagaceae, and Hyphomicrobiaceae (ρ = 0.17–0.25, P ≤ 0.041). Prokaryotic community composition accounted for the least amount of variation in denitrification rates (22%), while the collective influence of spatiotemporal factors and gene abundances accounted for 37%, with 40% of the variation related to interactions among all parameters. Results of this study suggest that the hydrologic connectivity at each location had a greater effect on the prokaryotic community than did spatiotemporal differences, where inundation is associated with shifts favoring increased denitrification potential. We further establish that while complex interactions among the prokaryotic community influence denitrification, the link between hydrologic connectivity, microbial community composition, and genetic potential for biogeochemical cycling is a promising avenue to explore hydrologic remediation strategies such as periodic flooding. Frontiers Media S.A. 2017-11-22 /pmc/articles/PMC5702768/ /pubmed/29213260 http://dx.doi.org/10.3389/fmicb.2017.02304 Text en Copyright © 2017 Tomasek, Staley, Wang, Kaiser, Lurndahl, Kozarek, Hondzo and Sadowsky. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Tomasek, Abigail
Staley, Christopher
Wang, Ping
Kaiser, Thomas
Lurndahl, Nicole
Kozarek, Jessica L.
Hondzo, Miki
Sadowsky, Michael J.
Increased Denitrification Rates Associated with Shifts in Prokaryotic Community Composition Caused by Varying Hydrologic Connectivity
title Increased Denitrification Rates Associated with Shifts in Prokaryotic Community Composition Caused by Varying Hydrologic Connectivity
title_full Increased Denitrification Rates Associated with Shifts in Prokaryotic Community Composition Caused by Varying Hydrologic Connectivity
title_fullStr Increased Denitrification Rates Associated with Shifts in Prokaryotic Community Composition Caused by Varying Hydrologic Connectivity
title_full_unstemmed Increased Denitrification Rates Associated with Shifts in Prokaryotic Community Composition Caused by Varying Hydrologic Connectivity
title_short Increased Denitrification Rates Associated with Shifts in Prokaryotic Community Composition Caused by Varying Hydrologic Connectivity
title_sort increased denitrification rates associated with shifts in prokaryotic community composition caused by varying hydrologic connectivity
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5702768/
https://www.ncbi.nlm.nih.gov/pubmed/29213260
http://dx.doi.org/10.3389/fmicb.2017.02304
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