Earthworm gut: An overlooked niche for anaerobic ammonium oxidation in agricultural soil

Soil fauna takes an active part in accelerating turnover of nutrients in terrestrial ecosystems. Anaerobic ammonium oxidation (anammox) has been widely characterized, however, whether anammox is active in earthworm gut and the effect of earthworm on anammox in soil remain unknown. In this study, the...

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Veröffentlicht in:The Science of the total environment 2021-01, Vol.752, p.141874-141874, Article 141874
Hauptverfasser: Li, Hu, Yang, Xiao-Ru, Wang, Juan, Zhou, Guo-Wei, Zhang, Yu-Sen, Lassen, Simon Bo, Zhu, Yong-Guan, Su, Jian-Qiang
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container_title The Science of the total environment
container_volume 752
creator Li, Hu
Yang, Xiao-Ru
Wang, Juan
Zhou, Guo-Wei
Zhang, Yu-Sen
Lassen, Simon Bo
Zhu, Yong-Guan
Su, Jian-Qiang
description Soil fauna takes an active part in accelerating turnover of nutrients in terrestrial ecosystems. Anaerobic ammonium oxidation (anammox) has been widely characterized, however, whether anammox is active in earthworm gut and the effect of earthworm on anammox in soil remain unknown. In this study, the activity, abundance and community of anammox bacteria in earthworm guts and soils from microcosms were determined using a 15N-tracing technique, quantitative PCR, and anammox bacterial 16S rRNA gene amplicon sequencing. Results showed that anammox rates in guts ranged between 5.81 and 14.19 nmol N g−1 dw gut content h−1, which were significantly (P 
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Anaerobic ammonium oxidation (anammox) has been widely characterized, however, whether anammox is active in earthworm gut and the effect of earthworm on anammox in soil remain unknown. In this study, the activity, abundance and community of anammox bacteria in earthworm guts and soils from microcosms were determined using a 15N-tracing technique, quantitative PCR, and anammox bacterial 16S rRNA gene amplicon sequencing. Results showed that anammox rates in guts ranged between 5.81 and 14.19 nmol N g−1 dw gut content h−1, which were significantly (P &lt; 0.01) higher than that in their surrounding soils during 30 day incubation. On the contrary, abundances of hzsB genes encoding subunit B hydrazine synthase in guts were significantly (P &lt; 0.05) lower than those in their surrounding soils. Anammox rates, denitrification N2 production rates and hzsB genes in soils with earthworms were significantly (P &lt; 0.05) lower than those in control soils. Anammox bacterial compositions differed significantly (P &lt; 0.05) between gut and soil, and earthworm altered anammox bacterial communities in soils. Brocadia, Kuenenia and abundant unclassified anammox bacteria were detected in collected soils and gut contents, in which Brocadia was only detected in guts. These results suggested that microbes in earthworm gut increase, but present of earthworm reduces anammox and denitrification associated N loss by altering the anammox bacterial community compositions in soils. [Display omitted] •Anammox rates in earthworm gut were significantly higher than those in soils.•Earthworm reduced the anammox and denitrification N2-producing rates in soils.•Anammox bacterial compositions in gut differed from those in soils.•Earthworm changed the anammox bacterial communities in soils.</description><identifier>ISSN: 0048-9697</identifier><identifier>EISSN: 1879-1026</identifier><identifier>DOI: 10.1016/j.scitotenv.2020.141874</identifier><language>eng</language><publisher>Elsevier B.V</publisher><subject>Agricultural soil ; agricultural soils ; anaerobic ammonium oxidation ; Anammox ; bacterial communities ; denitrification ; digestive system ; earthworms ; environment ; genes ; Gut microbiota ; hydrazine ; Nitrogen cycle ; quantitative polymerase chain reaction ; Soil fauna</subject><ispartof>The Science of the total environment, 2021-01, Vol.752, p.141874-141874, Article 141874</ispartof><rights>2020 Elsevier B.V.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c381t-47fe035cb212d1d45005789fe7491fa115f8fff5b0446d6c1916e282791fd3b53</citedby><cites>FETCH-LOGICAL-c381t-47fe035cb212d1d45005789fe7491fa115f8fff5b0446d6c1916e282791fd3b53</cites><orcidid>0000-0002-9781-1939 ; 0000-0001-5849-4400</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.scitotenv.2020.141874$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,778,782,3539,27911,27912,45982</link.rule.ids></links><search><creatorcontrib>Li, Hu</creatorcontrib><creatorcontrib>Yang, Xiao-Ru</creatorcontrib><creatorcontrib>Wang, Juan</creatorcontrib><creatorcontrib>Zhou, Guo-Wei</creatorcontrib><creatorcontrib>Zhang, Yu-Sen</creatorcontrib><creatorcontrib>Lassen, Simon Bo</creatorcontrib><creatorcontrib>Zhu, Yong-Guan</creatorcontrib><creatorcontrib>Su, Jian-Qiang</creatorcontrib><title>Earthworm gut: An overlooked niche for anaerobic ammonium oxidation in agricultural soil</title><title>The Science of the total environment</title><description>Soil fauna takes an active part in accelerating turnover of nutrients in terrestrial ecosystems. Anaerobic ammonium oxidation (anammox) has been widely characterized, however, whether anammox is active in earthworm gut and the effect of earthworm on anammox in soil remain unknown. In this study, the activity, abundance and community of anammox bacteria in earthworm guts and soils from microcosms were determined using a 15N-tracing technique, quantitative PCR, and anammox bacterial 16S rRNA gene amplicon sequencing. Results showed that anammox rates in guts ranged between 5.81 and 14.19 nmol N g−1 dw gut content h−1, which were significantly (P &lt; 0.01) higher than that in their surrounding soils during 30 day incubation. On the contrary, abundances of hzsB genes encoding subunit B hydrazine synthase in guts were significantly (P &lt; 0.05) lower than those in their surrounding soils. Anammox rates, denitrification N2 production rates and hzsB genes in soils with earthworms were significantly (P &lt; 0.05) lower than those in control soils. Anammox bacterial compositions differed significantly (P &lt; 0.05) between gut and soil, and earthworm altered anammox bacterial communities in soils. Brocadia, Kuenenia and abundant unclassified anammox bacteria were detected in collected soils and gut contents, in which Brocadia was only detected in guts. These results suggested that microbes in earthworm gut increase, but present of earthworm reduces anammox and denitrification associated N loss by altering the anammox bacterial community compositions in soils. [Display omitted] •Anammox rates in earthworm gut were significantly higher than those in soils.•Earthworm reduced the anammox and denitrification N2-producing rates in soils.•Anammox bacterial compositions in gut differed from those in soils.•Earthworm changed the anammox bacterial communities in soils.</description><subject>Agricultural soil</subject><subject>agricultural soils</subject><subject>anaerobic ammonium oxidation</subject><subject>Anammox</subject><subject>bacterial communities</subject><subject>denitrification</subject><subject>digestive system</subject><subject>earthworms</subject><subject>environment</subject><subject>genes</subject><subject>Gut microbiota</subject><subject>hydrazine</subject><subject>Nitrogen cycle</subject><subject>quantitative polymerase chain reaction</subject><subject>Soil fauna</subject><issn>0048-9697</issn><issn>1879-1026</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNqFkE9PAyEQxYnRxFr9DHL0shUoC6y3xvgvMfGiiTdC2aGl7oICW_Xbu02NV-fykpnfe8k8hM4pmVFCxeVmlq0vsUDYzhhh45ZTJfkBmozSVJQwcYgmhHBVNaKRx-gk5w0ZRyo6Qa83JpX1Z0w9Xg3lCi8CjltIXYxv0OLg7RqwiwmbYCDFpbfY9H0Mfuhx_PKtKT4G7AM2q-Tt0JUhmQ7n6LtTdORMl-HsV6fo5fbm-fq-eny6e7hePFZ2rmipuHRA5rVdMspa2vKakFqqxoHkDXWG0top51y9JJyLVljaUAFMMTle2_mynk_RxT73PcWPAXLRvc8Wus4EiEPWrFFCKcao-h_lnHAhRcNGVO5Rm2LOCZx-T7436VtTone1643-q13vatf72kfnYu-E8emth7TjIFhofQJbdBv9vxk_20CQQA</recordid><startdate>20210115</startdate><enddate>20210115</enddate><creator>Li, Hu</creator><creator>Yang, Xiao-Ru</creator><creator>Wang, Juan</creator><creator>Zhou, Guo-Wei</creator><creator>Zhang, Yu-Sen</creator><creator>Lassen, Simon Bo</creator><creator>Zhu, Yong-Guan</creator><creator>Su, Jian-Qiang</creator><general>Elsevier B.V</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0002-9781-1939</orcidid><orcidid>https://orcid.org/0000-0001-5849-4400</orcidid></search><sort><creationdate>20210115</creationdate><title>Earthworm gut: An overlooked niche for anaerobic ammonium oxidation in agricultural soil</title><author>Li, Hu ; Yang, Xiao-Ru ; Wang, Juan ; Zhou, Guo-Wei ; Zhang, Yu-Sen ; Lassen, Simon Bo ; Zhu, Yong-Guan ; Su, Jian-Qiang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c381t-47fe035cb212d1d45005789fe7491fa115f8fff5b0446d6c1916e282791fd3b53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Agricultural soil</topic><topic>agricultural soils</topic><topic>anaerobic ammonium oxidation</topic><topic>Anammox</topic><topic>bacterial communities</topic><topic>denitrification</topic><topic>digestive system</topic><topic>earthworms</topic><topic>environment</topic><topic>genes</topic><topic>Gut microbiota</topic><topic>hydrazine</topic><topic>Nitrogen cycle</topic><topic>quantitative polymerase chain reaction</topic><topic>Soil fauna</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Li, Hu</creatorcontrib><creatorcontrib>Yang, Xiao-Ru</creatorcontrib><creatorcontrib>Wang, Juan</creatorcontrib><creatorcontrib>Zhou, Guo-Wei</creatorcontrib><creatorcontrib>Zhang, Yu-Sen</creatorcontrib><creatorcontrib>Lassen, Simon Bo</creatorcontrib><creatorcontrib>Zhu, Yong-Guan</creatorcontrib><creatorcontrib>Su, Jian-Qiang</creatorcontrib><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>The Science of the total environment</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Li, Hu</au><au>Yang, Xiao-Ru</au><au>Wang, Juan</au><au>Zhou, Guo-Wei</au><au>Zhang, Yu-Sen</au><au>Lassen, Simon Bo</au><au>Zhu, Yong-Guan</au><au>Su, Jian-Qiang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Earthworm gut: An overlooked niche for anaerobic ammonium oxidation in agricultural soil</atitle><jtitle>The Science of the total environment</jtitle><date>2021-01-15</date><risdate>2021</risdate><volume>752</volume><spage>141874</spage><epage>141874</epage><pages>141874-141874</pages><artnum>141874</artnum><issn>0048-9697</issn><eissn>1879-1026</eissn><abstract>Soil fauna takes an active part in accelerating turnover of nutrients in terrestrial ecosystems. Anaerobic ammonium oxidation (anammox) has been widely characterized, however, whether anammox is active in earthworm gut and the effect of earthworm on anammox in soil remain unknown. In this study, the activity, abundance and community of anammox bacteria in earthworm guts and soils from microcosms were determined using a 15N-tracing technique, quantitative PCR, and anammox bacterial 16S rRNA gene amplicon sequencing. Results showed that anammox rates in guts ranged between 5.81 and 14.19 nmol N g−1 dw gut content h−1, which were significantly (P &lt; 0.01) higher than that in their surrounding soils during 30 day incubation. On the contrary, abundances of hzsB genes encoding subunit B hydrazine synthase in guts were significantly (P &lt; 0.05) lower than those in their surrounding soils. Anammox rates, denitrification N2 production rates and hzsB genes in soils with earthworms were significantly (P &lt; 0.05) lower than those in control soils. Anammox bacterial compositions differed significantly (P &lt; 0.05) between gut and soil, and earthworm altered anammox bacterial communities in soils. Brocadia, Kuenenia and abundant unclassified anammox bacteria were detected in collected soils and gut contents, in which Brocadia was only detected in guts. These results suggested that microbes in earthworm gut increase, but present of earthworm reduces anammox and denitrification associated N loss by altering the anammox bacterial community compositions in soils. [Display omitted] •Anammox rates in earthworm gut were significantly higher than those in soils.•Earthworm reduced the anammox and denitrification N2-producing rates in soils.•Anammox bacterial compositions in gut differed from those in soils.•Earthworm changed the anammox bacterial communities in soils.</abstract><pub>Elsevier B.V</pub><doi>10.1016/j.scitotenv.2020.141874</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-9781-1939</orcidid><orcidid>https://orcid.org/0000-0001-5849-4400</orcidid></addata></record>
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source ScienceDirect Journals (5 years ago - present)
subjects Agricultural soil
agricultural soils
anaerobic ammonium oxidation
Anammox
bacterial communities
denitrification
digestive system
earthworms
environment
genes
Gut microbiota
hydrazine
Nitrogen cycle
quantitative polymerase chain reaction
Soil fauna
title Earthworm gut: An overlooked niche for anaerobic ammonium oxidation in agricultural soil
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