Elucidating the links between N2O dynamics and changes in microbial communities following saltwater intrusions

Saltwater intrusion in estuarine ecosystems alters microbial communities as well as biogeochemical cycling processes and has become a worldwide problem. However, the impact of salinity intrusion on the dynamics of nitrous oxide (N2O) and associated microbial community are understudied. Here, we cond...

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Veröffentlicht in:Environmental research 2024-03, Vol.245, p.118021-118021, Article 118021
Hauptverfasser: Xie, Rongrong, Lin, Laichang, Shi, Chengchun, Zhang, Peng, Rao, Peiyuan, Li, Jiabing, Izabel-Shen, Dandan
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container_title Environmental research
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creator Xie, Rongrong
Lin, Laichang
Shi, Chengchun
Zhang, Peng
Rao, Peiyuan
Li, Jiabing
Izabel-Shen, Dandan
description Saltwater intrusion in estuarine ecosystems alters microbial communities as well as biogeochemical cycling processes and has become a worldwide problem. However, the impact of salinity intrusion on the dynamics of nitrous oxide (N2O) and associated microbial community are understudied. Here, we conducted field microcosms in a tidal estuary during different months (December, April and August) using dialysis bags, and microbes inside the bags encountered a change in salinity in natural setting. We then compared N2O dynamics in the microcosms with that in natural water. Regardless of incubation environment, saltwater intrusion altered the dissolved N2O depending on the initial saturation rates of N2O. While the impact of saltwater intrusion on N2O dynamics was consistent across months, the dissolved N2O was higher in summer than in winter. The N-related microbial communities following saltwater intrusion were dominated by denitrifers, with fewer nitrifiers and bacterial taxa involved in dissimilatory nitrate reduction to ammonium. While denitrification was a significant driver of N2O dynamics in the studied estuary, nitrifier-involved denitrification contributed to the additional production of N2O, evidenced by the strong associations with amoA genes and the abundance of Nitrospira. Higher N2O concentrations in the field microcosms than in natural water limited N2O consumption in the former, given the lack of an association with nosZ gene abundance. The differences in the N2O dynamics observed between the microcosms and natural water could be that the latter comprised not only indigenous microbes but also those accompanied with saltwater intrusion, and that immigrants might be functionally rich individuals and able to perform N transformation in multiple pathways. Our work provides the first quantitative assessment of in situ N2O concentrations in an estuary subjected to a saltwater intrusion. The results highlight the importance of ecosystem size and microbial connectivity in the source-sink dynamics of N2O in changing environments. [Display omitted] •N2O changes following saltwater intrusion depended on its initial saturation rate.•Dissolved N2O concentration was higher in summer than in winter.•Microbes harbored more denitrifiers and fewer nitrifiers after saltwater inflow.•An additional source of N2O production is attributed to nitrifier denitrification.•Higher N2O in the field microcosms than natural water was due to low consumption.
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However, the impact of salinity intrusion on the dynamics of nitrous oxide (N2O) and associated microbial community are understudied. Here, we conducted field microcosms in a tidal estuary during different months (December, April and August) using dialysis bags, and microbes inside the bags encountered a change in salinity in natural setting. We then compared N2O dynamics in the microcosms with that in natural water. Regardless of incubation environment, saltwater intrusion altered the dissolved N2O depending on the initial saturation rates of N2O. While the impact of saltwater intrusion on N2O dynamics was consistent across months, the dissolved N2O was higher in summer than in winter. The N-related microbial communities following saltwater intrusion were dominated by denitrifers, with fewer nitrifiers and bacterial taxa involved in dissimilatory nitrate reduction to ammonium. While denitrification was a significant driver of N2O dynamics in the studied estuary, nitrifier-involved denitrification contributed to the additional production of N2O, evidenced by the strong associations with amoA genes and the abundance of Nitrospira. Higher N2O concentrations in the field microcosms than in natural water limited N2O consumption in the former, given the lack of an association with nosZ gene abundance. The differences in the N2O dynamics observed between the microcosms and natural water could be that the latter comprised not only indigenous microbes but also those accompanied with saltwater intrusion, and that immigrants might be functionally rich individuals and able to perform N transformation in multiple pathways. Our work provides the first quantitative assessment of in situ N2O concentrations in an estuary subjected to a saltwater intrusion. 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[Display omitted] •N2O changes following saltwater intrusion depended on its initial saturation rate.•Dissolved N2O concentration was higher in summer than in winter.•Microbes harbored more denitrifiers and fewer nitrifiers after saltwater inflow.•An additional source of N2O production is attributed to nitrifier denitrification.•Higher N2O in the field microcosms than natural water was due to low consumption.</description><identifier>ISSN: 0013-9351</identifier><identifier>EISSN: 1096-0953</identifier><identifier>DOI: 10.1016/j.envres.2023.118021</identifier><language>eng</language><publisher>Elsevier Inc</publisher><subject>ammonium ; Denitrification ; dialysis ; ecosystems ; estuaries ; Estuary ; genes ; Greenhouse gases ; microbial communities ; Microbial community ; nitrate reduction ; Nitrogen gene ; nitrous oxide ; saline water ; salinity ; saltwater intrusion ; summer ; winter</subject><ispartof>Environmental research, 2024-03, Vol.245, p.118021-118021, Article 118021</ispartof><rights>2023 Elsevier Inc.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c321t-524987d585ce62fc44f7002b8893630452a0df09a58f1b9ebb9aaae1ba1f5c823</cites><orcidid>0000-0002-2739-1107</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0013935123028256$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids></links><search><creatorcontrib>Xie, Rongrong</creatorcontrib><creatorcontrib>Lin, Laichang</creatorcontrib><creatorcontrib>Shi, Chengchun</creatorcontrib><creatorcontrib>Zhang, Peng</creatorcontrib><creatorcontrib>Rao, Peiyuan</creatorcontrib><creatorcontrib>Li, Jiabing</creatorcontrib><creatorcontrib>Izabel-Shen, Dandan</creatorcontrib><title>Elucidating the links between N2O dynamics and changes in microbial communities following saltwater intrusions</title><title>Environmental research</title><description>Saltwater intrusion in estuarine ecosystems alters microbial communities as well as biogeochemical cycling processes and has become a worldwide problem. 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While denitrification was a significant driver of N2O dynamics in the studied estuary, nitrifier-involved denitrification contributed to the additional production of N2O, evidenced by the strong associations with amoA genes and the abundance of Nitrospira. Higher N2O concentrations in the field microcosms than in natural water limited N2O consumption in the former, given the lack of an association with nosZ gene abundance. The differences in the N2O dynamics observed between the microcosms and natural water could be that the latter comprised not only indigenous microbes but also those accompanied with saltwater intrusion, and that immigrants might be functionally rich individuals and able to perform N transformation in multiple pathways. Our work provides the first quantitative assessment of in situ N2O concentrations in an estuary subjected to a saltwater intrusion. The results highlight the importance of ecosystem size and microbial connectivity in the source-sink dynamics of N2O in changing environments. [Display omitted] •N2O changes following saltwater intrusion depended on its initial saturation rate.•Dissolved N2O concentration was higher in summer than in winter.•Microbes harbored more denitrifiers and fewer nitrifiers after saltwater inflow.•An additional source of N2O production is attributed to nitrifier denitrification.•Higher N2O in the field microcosms than natural water was due to low consumption.</description><subject>ammonium</subject><subject>Denitrification</subject><subject>dialysis</subject><subject>ecosystems</subject><subject>estuaries</subject><subject>Estuary</subject><subject>genes</subject><subject>Greenhouse gases</subject><subject>microbial communities</subject><subject>Microbial community</subject><subject>nitrate reduction</subject><subject>Nitrogen gene</subject><subject>nitrous oxide</subject><subject>saline water</subject><subject>salinity</subject><subject>saltwater intrusion</subject><subject>summer</subject><subject>winter</subject><issn>0013-9351</issn><issn>1096-0953</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNqFkUFr3DAQhUVJoZtt_0EPOubi7UiyvNIlEEKSFkJyac9ClseJtrKcSnKW_Ptqcc_NaZiZ7z14PEK-MtgxYN23ww7ja8K848DFjjEFnH0gGwa6a0BLcUY2AEw0Wkj2iZznfKgrkwI2JN6ExfnBFh-faHlGGnz8nWmP5YgY6QN_pMNbtJN3mdo4UPds4xNm6iOttzT33gbq5mlaoi--PsY5hPl4css2lKMtmCpc0pL9HPNn8nG0IeOXf3NLft3e_Lz-3tw_3v24vrpvnOCsNJK3Wu0HqaTDjo-ubcc9AO-V0qIT0EpuYRhBW6lG1mvse22tRdZbNkqnuNiSi9X3Jc1_FszFTD47DMFGnJdsRE3fgeItvItyDd1-L9pOVbRd0Ro854SjeUl-sunNMDCnJszBrE2YUxNmbaLKLlcZ1sSvHpPJzmN0OPiErphh9v83-AvF15Ud</recordid><startdate>20240315</startdate><enddate>20240315</enddate><creator>Xie, Rongrong</creator><creator>Lin, Laichang</creator><creator>Shi, Chengchun</creator><creator>Zhang, Peng</creator><creator>Rao, Peiyuan</creator><creator>Li, Jiabing</creator><creator>Izabel-Shen, Dandan</creator><general>Elsevier Inc</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0002-2739-1107</orcidid></search><sort><creationdate>20240315</creationdate><title>Elucidating the links between N2O dynamics and changes in microbial communities following saltwater intrusions</title><author>Xie, Rongrong ; Lin, Laichang ; Shi, Chengchun ; Zhang, Peng ; Rao, Peiyuan ; Li, Jiabing ; Izabel-Shen, Dandan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c321t-524987d585ce62fc44f7002b8893630452a0df09a58f1b9ebb9aaae1ba1f5c823</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>ammonium</topic><topic>Denitrification</topic><topic>dialysis</topic><topic>ecosystems</topic><topic>estuaries</topic><topic>Estuary</topic><topic>genes</topic><topic>Greenhouse gases</topic><topic>microbial communities</topic><topic>Microbial community</topic><topic>nitrate reduction</topic><topic>Nitrogen gene</topic><topic>nitrous oxide</topic><topic>saline water</topic><topic>salinity</topic><topic>saltwater intrusion</topic><topic>summer</topic><topic>winter</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Xie, Rongrong</creatorcontrib><creatorcontrib>Lin, Laichang</creatorcontrib><creatorcontrib>Shi, Chengchun</creatorcontrib><creatorcontrib>Zhang, Peng</creatorcontrib><creatorcontrib>Rao, Peiyuan</creatorcontrib><creatorcontrib>Li, Jiabing</creatorcontrib><creatorcontrib>Izabel-Shen, Dandan</creatorcontrib><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Environmental research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Xie, Rongrong</au><au>Lin, Laichang</au><au>Shi, Chengchun</au><au>Zhang, Peng</au><au>Rao, Peiyuan</au><au>Li, Jiabing</au><au>Izabel-Shen, Dandan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Elucidating the links between N2O dynamics and changes in microbial communities following saltwater intrusions</atitle><jtitle>Environmental research</jtitle><date>2024-03-15</date><risdate>2024</risdate><volume>245</volume><spage>118021</spage><epage>118021</epage><pages>118021-118021</pages><artnum>118021</artnum><issn>0013-9351</issn><eissn>1096-0953</eissn><abstract>Saltwater intrusion in estuarine ecosystems alters microbial communities as well as biogeochemical cycling processes and has become a worldwide problem. However, the impact of salinity intrusion on the dynamics of nitrous oxide (N2O) and associated microbial community are understudied. Here, we conducted field microcosms in a tidal estuary during different months (December, April and August) using dialysis bags, and microbes inside the bags encountered a change in salinity in natural setting. We then compared N2O dynamics in the microcosms with that in natural water. Regardless of incubation environment, saltwater intrusion altered the dissolved N2O depending on the initial saturation rates of N2O. While the impact of saltwater intrusion on N2O dynamics was consistent across months, the dissolved N2O was higher in summer than in winter. The N-related microbial communities following saltwater intrusion were dominated by denitrifers, with fewer nitrifiers and bacterial taxa involved in dissimilatory nitrate reduction to ammonium. While denitrification was a significant driver of N2O dynamics in the studied estuary, nitrifier-involved denitrification contributed to the additional production of N2O, evidenced by the strong associations with amoA genes and the abundance of Nitrospira. Higher N2O concentrations in the field microcosms than in natural water limited N2O consumption in the former, given the lack of an association with nosZ gene abundance. The differences in the N2O dynamics observed between the microcosms and natural water could be that the latter comprised not only indigenous microbes but also those accompanied with saltwater intrusion, and that immigrants might be functionally rich individuals and able to perform N transformation in multiple pathways. Our work provides the first quantitative assessment of in situ N2O concentrations in an estuary subjected to a saltwater intrusion. The results highlight the importance of ecosystem size and microbial connectivity in the source-sink dynamics of N2O in changing environments. [Display omitted] •N2O changes following saltwater intrusion depended on its initial saturation rate.•Dissolved N2O concentration was higher in summer than in winter.•Microbes harbored more denitrifiers and fewer nitrifiers after saltwater inflow.•An additional source of N2O production is attributed to nitrifier denitrification.•Higher N2O in the field microcosms than natural water was due to low consumption.</abstract><pub>Elsevier Inc</pub><doi>10.1016/j.envres.2023.118021</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-2739-1107</orcidid></addata></record>
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subjects ammonium
Denitrification
dialysis
ecosystems
estuaries
Estuary
genes
Greenhouse gases
microbial communities
Microbial community
nitrate reduction
Nitrogen gene
nitrous oxide
saline water
salinity
saltwater intrusion
summer
winter
title Elucidating the links between N2O dynamics and changes in microbial communities following saltwater intrusions
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