Exploring bacterial community structure and function associated with polychlorinated biphenyl biodegradation in two hydrogen-amended soils

Hydrogen (H2) is a universal energy source supplying survival energy for numerous microbial functions. Diffusive fluxes of H2 released by rhizobacterial symbiont nodules in which H2 is an obligate by-product of dinitrogen fixation may act as an additional energy input shaping microbial community str...

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Veröffentlicht in:The Science of the total environment 2020-11, Vol.745, p.140839-140839, Article 140839
Hauptverfasser: Xu, Yongfeng, Teng, Ying, Wang, Xiaomi, Li, Ran, Christie, Peter
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Teng, Ying
Wang, Xiaomi
Li, Ran
Christie, Peter
description Hydrogen (H2) is a universal energy source supplying survival energy for numerous microbial functions. Diffusive fluxes of H2 released by rhizobacterial symbiont nodules in which H2 is an obligate by-product of dinitrogen fixation may act as an additional energy input shaping microbial community structure and function in soils. However, the effects of H2 at the soil-nodule interface on soil contaminant degradation processes are poorly understood. Here, we mimicked the hydrogen conditions present at the soil-nodule interface (10,000 ppmv) to test the impact of elevated H2 concentrations on soil microbial removal of 3, 3′, 4, 4′-tetrachlorobiphenyl (PCB77) and examined the associated bacterial communities and their functions by conducting a microcosm experiment using two different soil types at three PCB contamination levels (0.5, 1.0 and 5.0 mg kg−1). After incubation for 84 days the PCB77 removal rates in the elevated H2 treatments in the Paddy soil were significantly promoted (by 4.88 to 6.41%) compared with the control (0.5 ppmv H2) but no significant effect was observed in a Fluvo-aquic soil. This is consistent with changes in the abundance of functional genes for PCB-degraders as shown by quantitative real-time PCR (Q-PCR) and phylogenetic investigation of bacterial communities by reconstruction of unobserved states (PICRUSt). 16S amplicon sequencing was conducted to explore bacterial community structure and correlate the genera to potential PCB degradation. The abundance of a total of four potentially PCB-degrading bacterial genera (Bacillus, Streptomyces, Ramlibacter and Paenibacillus) increased with increasing H2 level. In addition, the abundance of hydrogenase in the elevated H2 treatments was higher than in the control across different contamination levels in both soil types. Thus, elevated H2 stimulated soil PCB degradation with direct effects (aerobic PCB-degrading bacteria directly utilized H2 as an energy source for growth and thus enhanced PCB degradation efficiency) and indirect effects (aerobic PCB-degrading bacteria acted synergistically with other hydrogenotrophs to enhance PCB degradation efficiency by exchange of substances and energy). These results help to further understand the role of elevated hydrogen amendment in the PCB biodegradation process and provide evidence that H2 supports metabolic and energetic flexibility in microorganisms supplying a range of ecosystem services. [Display omitted] •Elevated H2 could modify the PCB77 dis
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Diffusive fluxes of H2 released by rhizobacterial symbiont nodules in which H2 is an obligate by-product of dinitrogen fixation may act as an additional energy input shaping microbial community structure and function in soils. However, the effects of H2 at the soil-nodule interface on soil contaminant degradation processes are poorly understood. Here, we mimicked the hydrogen conditions present at the soil-nodule interface (10,000 ppmv) to test the impact of elevated H2 concentrations on soil microbial removal of 3, 3′, 4, 4′-tetrachlorobiphenyl (PCB77) and examined the associated bacterial communities and their functions by conducting a microcosm experiment using two different soil types at three PCB contamination levels (0.5, 1.0 and 5.0 mg kg−1). After incubation for 84 days the PCB77 removal rates in the elevated H2 treatments in the Paddy soil were significantly promoted (by 4.88 to 6.41%) compared with the control (0.5 ppmv H2) but no significant effect was observed in a Fluvo-aquic soil. This is consistent with changes in the abundance of functional genes for PCB-degraders as shown by quantitative real-time PCR (Q-PCR) and phylogenetic investigation of bacterial communities by reconstruction of unobserved states (PICRUSt). 16S amplicon sequencing was conducted to explore bacterial community structure and correlate the genera to potential PCB degradation. The abundance of a total of four potentially PCB-degrading bacterial genera (Bacillus, Streptomyces, Ramlibacter and Paenibacillus) increased with increasing H2 level. In addition, the abundance of hydrogenase in the elevated H2 treatments was higher than in the control across different contamination levels in both soil types. Thus, elevated H2 stimulated soil PCB degradation with direct effects (aerobic PCB-degrading bacteria directly utilized H2 as an energy source for growth and thus enhanced PCB degradation efficiency) and indirect effects (aerobic PCB-degrading bacteria acted synergistically with other hydrogenotrophs to enhance PCB degradation efficiency by exchange of substances and energy). These results help to further understand the role of elevated hydrogen amendment in the PCB biodegradation process and provide evidence that H2 supports metabolic and energetic flexibility in microorganisms supplying a range of ecosystem services. [Display omitted] •Elevated H2 could modify the PCB77 dissipation processes in soil.•Differences in PCB77 degradation rate were associated with soil type and bacterial enrichment.•Abundance of four genera increased after elevated H2 amendment.•PCB77 degradation in soil might be determined by interrelationship between functional microorganisms.</description><identifier>ISSN: 0048-9697</identifier><identifier>EISSN: 1879-1026</identifier><identifier>DOI: 10.1016/j.scitotenv.2020.140839</identifier><language>eng</language><publisher>Elsevier B.V</publisher><subject>Biodegradation ; Functional genes ; Hydrogen ; Microbial communities ; Synergistic effect</subject><ispartof>The Science of the total environment, 2020-11, Vol.745, p.140839-140839, Article 140839</ispartof><rights>2020 Elsevier B.V.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c348t-41ce966fca7278569e358a1cbfe66748c69e840c9e3582887df4448227c5735d3</citedby><cites>FETCH-LOGICAL-c348t-41ce966fca7278569e358a1cbfe66748c69e840c9e3582887df4448227c5735d3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.scitotenv.2020.140839$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>315,781,785,3551,27926,27927,45997</link.rule.ids></links><search><creatorcontrib>Xu, Yongfeng</creatorcontrib><creatorcontrib>Teng, Ying</creatorcontrib><creatorcontrib>Wang, Xiaomi</creatorcontrib><creatorcontrib>Li, Ran</creatorcontrib><creatorcontrib>Christie, Peter</creatorcontrib><title>Exploring bacterial community structure and function associated with polychlorinated biphenyl biodegradation in two hydrogen-amended soils</title><title>The Science of the total environment</title><description>Hydrogen (H2) is a universal energy source supplying survival energy for numerous microbial functions. Diffusive fluxes of H2 released by rhizobacterial symbiont nodules in which H2 is an obligate by-product of dinitrogen fixation may act as an additional energy input shaping microbial community structure and function in soils. However, the effects of H2 at the soil-nodule interface on soil contaminant degradation processes are poorly understood. Here, we mimicked the hydrogen conditions present at the soil-nodule interface (10,000 ppmv) to test the impact of elevated H2 concentrations on soil microbial removal of 3, 3′, 4, 4′-tetrachlorobiphenyl (PCB77) and examined the associated bacterial communities and their functions by conducting a microcosm experiment using two different soil types at three PCB contamination levels (0.5, 1.0 and 5.0 mg kg−1). After incubation for 84 days the PCB77 removal rates in the elevated H2 treatments in the Paddy soil were significantly promoted (by 4.88 to 6.41%) compared with the control (0.5 ppmv H2) but no significant effect was observed in a Fluvo-aquic soil. This is consistent with changes in the abundance of functional genes for PCB-degraders as shown by quantitative real-time PCR (Q-PCR) and phylogenetic investigation of bacterial communities by reconstruction of unobserved states (PICRUSt). 16S amplicon sequencing was conducted to explore bacterial community structure and correlate the genera to potential PCB degradation. The abundance of a total of four potentially PCB-degrading bacterial genera (Bacillus, Streptomyces, Ramlibacter and Paenibacillus) increased with increasing H2 level. In addition, the abundance of hydrogenase in the elevated H2 treatments was higher than in the control across different contamination levels in both soil types. 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[Display omitted] •Elevated H2 could modify the PCB77 dissipation processes in soil.•Differences in PCB77 degradation rate were associated with soil type and bacterial enrichment.•Abundance of four genera increased after elevated H2 amendment.•PCB77 degradation in soil might be determined by interrelationship between functional microorganisms.</description><subject>Biodegradation</subject><subject>Functional genes</subject><subject>Hydrogen</subject><subject>Microbial communities</subject><subject>Synergistic effect</subject><issn>0048-9697</issn><issn>1879-1026</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><recordid>eNqFkM1u2zAQhImiBeqmfYbymIsckqJE6hgE6Q8QIJf0TNDLlU1DIhWSSqpX6FNXtoNeu5ddfJgZYIeQr5xtOePtzXGbwZdYMLxsBRMrlUzX3Tuy4Vp1FWeifU82jElddW2nPpJPOR_ZOkrzDflz_3saYvJhT3cWCiZvBwpxHOfgy0JzSTOUOSG1wdF-DlB8DNTmHMHbgo6--nKgUxwWOJxzznDnpwOGZViP6HCfrLNnnw-0vEZ6WFyKewyVHTG4VZ-jH_Jn8qG3Q8Yvb_uK_Pp2_3T3o3p4_P7z7vahglrqUkkO2LVtD1YJpZu2w7rRlsOux7ZVUsNKtGRw5kJr5XoppRZCQaPqxtVX5PqSO6X4PGMuZvQZcBhswDhnI6ToWCOVlqtUXaSQYs4JezMlP9q0GM7MqX1zNP_aN6f2zaX91Xl7ceL6yYvHdNJhAHQ-IRTjov9vxl-FR5a6</recordid><startdate>20201125</startdate><enddate>20201125</enddate><creator>Xu, Yongfeng</creator><creator>Teng, Ying</creator><creator>Wang, Xiaomi</creator><creator>Li, Ran</creator><creator>Christie, Peter</creator><general>Elsevier B.V</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>20201125</creationdate><title>Exploring bacterial community structure and function associated with polychlorinated biphenyl biodegradation in two hydrogen-amended soils</title><author>Xu, Yongfeng ; Teng, Ying ; Wang, Xiaomi ; Li, Ran ; Christie, Peter</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c348t-41ce966fca7278569e358a1cbfe66748c69e840c9e3582887df4448227c5735d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Biodegradation</topic><topic>Functional genes</topic><topic>Hydrogen</topic><topic>Microbial communities</topic><topic>Synergistic effect</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Xu, Yongfeng</creatorcontrib><creatorcontrib>Teng, Ying</creatorcontrib><creatorcontrib>Wang, Xiaomi</creatorcontrib><creatorcontrib>Li, Ran</creatorcontrib><creatorcontrib>Christie, Peter</creatorcontrib><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>The Science of the total environment</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Xu, Yongfeng</au><au>Teng, Ying</au><au>Wang, Xiaomi</au><au>Li, Ran</au><au>Christie, Peter</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Exploring bacterial community structure and function associated with polychlorinated biphenyl biodegradation in two hydrogen-amended soils</atitle><jtitle>The Science of the total environment</jtitle><date>2020-11-25</date><risdate>2020</risdate><volume>745</volume><spage>140839</spage><epage>140839</epage><pages>140839-140839</pages><artnum>140839</artnum><issn>0048-9697</issn><eissn>1879-1026</eissn><abstract>Hydrogen (H2) is a universal energy source supplying survival energy for numerous microbial functions. Diffusive fluxes of H2 released by rhizobacterial symbiont nodules in which H2 is an obligate by-product of dinitrogen fixation may act as an additional energy input shaping microbial community structure and function in soils. However, the effects of H2 at the soil-nodule interface on soil contaminant degradation processes are poorly understood. Here, we mimicked the hydrogen conditions present at the soil-nodule interface (10,000 ppmv) to test the impact of elevated H2 concentrations on soil microbial removal of 3, 3′, 4, 4′-tetrachlorobiphenyl (PCB77) and examined the associated bacterial communities and their functions by conducting a microcosm experiment using two different soil types at three PCB contamination levels (0.5, 1.0 and 5.0 mg kg−1). After incubation for 84 days the PCB77 removal rates in the elevated H2 treatments in the Paddy soil were significantly promoted (by 4.88 to 6.41%) compared with the control (0.5 ppmv H2) but no significant effect was observed in a Fluvo-aquic soil. This is consistent with changes in the abundance of functional genes for PCB-degraders as shown by quantitative real-time PCR (Q-PCR) and phylogenetic investigation of bacterial communities by reconstruction of unobserved states (PICRUSt). 16S amplicon sequencing was conducted to explore bacterial community structure and correlate the genera to potential PCB degradation. The abundance of a total of four potentially PCB-degrading bacterial genera (Bacillus, Streptomyces, Ramlibacter and Paenibacillus) increased with increasing H2 level. In addition, the abundance of hydrogenase in the elevated H2 treatments was higher than in the control across different contamination levels in both soil types. Thus, elevated H2 stimulated soil PCB degradation with direct effects (aerobic PCB-degrading bacteria directly utilized H2 as an energy source for growth and thus enhanced PCB degradation efficiency) and indirect effects (aerobic PCB-degrading bacteria acted synergistically with other hydrogenotrophs to enhance PCB degradation efficiency by exchange of substances and energy). These results help to further understand the role of elevated hydrogen amendment in the PCB biodegradation process and provide evidence that H2 supports metabolic and energetic flexibility in microorganisms supplying a range of ecosystem services. [Display omitted] •Elevated H2 could modify the PCB77 dissipation processes in soil.•Differences in PCB77 degradation rate were associated with soil type and bacterial enrichment.•Abundance of four genera increased after elevated H2 amendment.•PCB77 degradation in soil might be determined by interrelationship between functional microorganisms.</abstract><pub>Elsevier B.V</pub><doi>10.1016/j.scitotenv.2020.140839</doi><tpages>1</tpages></addata></record>
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subjects Biodegradation
Functional genes
Hydrogen
Microbial communities
Synergistic effect
title Exploring bacterial community structure and function associated with polychlorinated biphenyl biodegradation in two hydrogen-amended soils
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