Plant-associated fungi support bacterial resilience following water limitation
Drought disrupts soil microbial activity and many biogeochemical processes. Although plant-associated fungi can support plant performance and nutrient cycling during drought, their effects on nearby drought-exposed soil microbial communities are not well resolved. We used H 2 18 O quantitative stabl...
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creator | Hestrin, Rachel Kan, Megan Lafler, Marissa Wollard, Jessica Kimbrel, Jeffrey A. Ray, Prasun Blazewicz, Steven J. Stuart, Rhona Craven, Kelly Firestone, Mary Nuccio, Erin E. Pett-Ridge, Jennifer |
description | Drought disrupts soil microbial activity and many biogeochemical processes. Although plant-associated fungi can support plant performance and nutrient cycling during drought, their effects on nearby drought-exposed soil microbial communities are not well resolved. We used H
2
18
O quantitative stable isotope probing (qSIP) and 16S rRNA gene profiling to investigate bacterial community dynamics following water limitation in the hyphospheres of two distinct fungal lineages (
Rhizophagus irregularis
and
Serendipita bescii
) grown with the bioenergy model grass
Panicum hallii
. In uninoculated soil, a history of water limitation resulted in significantly lower bacterial growth potential and growth efficiency, as well as lower diversity in the actively growing bacterial community. In contrast, both fungal lineages had a protective effect on hyphosphere bacterial communities exposed to water limitation: bacterial growth potential, growth efficiency, and the diversity of the actively growing bacterial community were not suppressed by a history of water limitation in soils inoculated with either fungus. Despite their similar effects at the community level, the two fungal lineages did elicit different taxon-specific responses, and bacterial growth potential was greater in
R. irregularis
compared to
S. bescii
-inoculated soils. Several of the bacterial taxa that responded positively to fungal inocula belong to lineages that are considered drought susceptible. Overall, H
2
18
O qSIP highlighted treatment effects on bacterial community structure that were less pronounced using traditional 16S rRNA gene profiling. Together, these results indicate that fungal–bacterial synergies may support bacterial resilience to moisture limitation. |
doi_str_mv | 10.1038/s41396-022-01308-6 |
format | Article |
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2
18
O quantitative stable isotope probing (qSIP) and 16S rRNA gene profiling to investigate bacterial community dynamics following water limitation in the hyphospheres of two distinct fungal lineages (
Rhizophagus irregularis
and
Serendipita bescii
) grown with the bioenergy model grass
Panicum hallii
. In uninoculated soil, a history of water limitation resulted in significantly lower bacterial growth potential and growth efficiency, as well as lower diversity in the actively growing bacterial community. In contrast, both fungal lineages had a protective effect on hyphosphere bacterial communities exposed to water limitation: bacterial growth potential, growth efficiency, and the diversity of the actively growing bacterial community were not suppressed by a history of water limitation in soils inoculated with either fungus. Despite their similar effects at the community level, the two fungal lineages did elicit different taxon-specific responses, and bacterial growth potential was greater in
R. irregularis
compared to
S. bescii
-inoculated soils. Several of the bacterial taxa that responded positively to fungal inocula belong to lineages that are considered drought susceptible. Overall, H
2
18
O qSIP highlighted treatment effects on bacterial community structure that were less pronounced using traditional 16S rRNA gene profiling. Together, these results indicate that fungal–bacterial synergies may support bacterial resilience to moisture limitation.</description><identifier>ISSN: 1751-7362</identifier><identifier>ISSN: 1751-7370</identifier><identifier>EISSN: 1751-7370</identifier><identifier>DOI: 10.1038/s41396-022-01308-6</identifier><identifier>PMID: 36085516</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>45 ; 45/23 ; 45/77 ; 631/1647/514/1948 ; 631/326/193/2539 ; 631/326/2565/855 ; 704/158/2165 ; 704/158/2466 ; Bacteria ; Biogeochemistry ; Biological activity ; Biomedical and Life Sciences ; Community structure ; Drought ; Ecology ; Evolutionary Biology ; Fungi ; Life Sciences ; Microbial activity ; Microbial Ecology ; Microbial Genetics and Genomics ; Microbiology ; Microorganisms ; Moisture effects ; Nutrient cycles ; Plant growth ; Resilience ; RNA, Ribosomal, 16S - genetics ; rRNA 16S ; Soil - chemistry ; Soil Microbiology ; Soil microorganisms ; Soil water ; Soils ; Stable isotopes ; Water - analysis</subject><ispartof>The ISME Journal, 2022-12, Vol.16 (12), p.2752-2762</ispartof><rights>The Author(s) 2022</rights><rights>2022. The Author(s).</rights><rights>The Author(s) 2022. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c501t-e1afbd3f685b17c0a9985cc76a9b34d545bfec89ef760e6f2a3fceb3bcdfe2273</citedby><cites>FETCH-LOGICAL-c501t-e1afbd3f685b17c0a9985cc76a9b34d545bfec89ef760e6f2a3fceb3bcdfe2273</cites><orcidid>0000-0003-1315-8870 ; 0000-0001-5916-9693 ; 0000-0002-4439-2398 ; 0000-0002-9329-2609 ; 0000-0001-7517-1750 ; 0000-0001-7213-9392 ; 0000-0003-0189-183X ; 0000-0002-0526-0130 ; 0000000172139392 ; 0000000293292609 ; 0000000205260130 ; 000000030189183X ; 0000000244392398 ; 0000000175171750 ; 0000000313158870 ; 0000000159169693</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9666503/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9666503/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36085516$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/biblio/1886421$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Hestrin, Rachel</creatorcontrib><creatorcontrib>Kan, Megan</creatorcontrib><creatorcontrib>Lafler, Marissa</creatorcontrib><creatorcontrib>Wollard, Jessica</creatorcontrib><creatorcontrib>Kimbrel, Jeffrey A.</creatorcontrib><creatorcontrib>Ray, Prasun</creatorcontrib><creatorcontrib>Blazewicz, Steven J.</creatorcontrib><creatorcontrib>Stuart, Rhona</creatorcontrib><creatorcontrib>Craven, Kelly</creatorcontrib><creatorcontrib>Firestone, Mary</creatorcontrib><creatorcontrib>Nuccio, Erin E.</creatorcontrib><creatorcontrib>Pett-Ridge, Jennifer</creatorcontrib><title>Plant-associated fungi support bacterial resilience following water limitation</title><title>The ISME Journal</title><addtitle>ISME J</addtitle><addtitle>ISME J</addtitle><description>Drought disrupts soil microbial activity and many biogeochemical processes. Although plant-associated fungi can support plant performance and nutrient cycling during drought, their effects on nearby drought-exposed soil microbial communities are not well resolved. We used H
2
18
O quantitative stable isotope probing (qSIP) and 16S rRNA gene profiling to investigate bacterial community dynamics following water limitation in the hyphospheres of two distinct fungal lineages (
Rhizophagus irregularis
and
Serendipita bescii
) grown with the bioenergy model grass
Panicum hallii
. In uninoculated soil, a history of water limitation resulted in significantly lower bacterial growth potential and growth efficiency, as well as lower diversity in the actively growing bacterial community. In contrast, both fungal lineages had a protective effect on hyphosphere bacterial communities exposed to water limitation: bacterial growth potential, growth efficiency, and the diversity of the actively growing bacterial community were not suppressed by a history of water limitation in soils inoculated with either fungus. Despite their similar effects at the community level, the two fungal lineages did elicit different taxon-specific responses, and bacterial growth potential was greater in
R. irregularis
compared to
S. bescii
-inoculated soils. Several of the bacterial taxa that responded positively to fungal inocula belong to lineages that are considered drought susceptible. Overall, H
2
18
O qSIP highlighted treatment effects on bacterial community structure that were less pronounced using traditional 16S rRNA gene profiling. Together, these results indicate that fungal–bacterial synergies may support bacterial resilience to moisture limitation.</description><subject>45</subject><subject>45/23</subject><subject>45/77</subject><subject>631/1647/514/1948</subject><subject>631/326/193/2539</subject><subject>631/326/2565/855</subject><subject>704/158/2165</subject><subject>704/158/2466</subject><subject>Bacteria</subject><subject>Biogeochemistry</subject><subject>Biological activity</subject><subject>Biomedical and Life Sciences</subject><subject>Community structure</subject><subject>Drought</subject><subject>Ecology</subject><subject>Evolutionary Biology</subject><subject>Fungi</subject><subject>Life Sciences</subject><subject>Microbial activity</subject><subject>Microbial Ecology</subject><subject>Microbial Genetics and Genomics</subject><subject>Microbiology</subject><subject>Microorganisms</subject><subject>Moisture effects</subject><subject>Nutrient cycles</subject><subject>Plant 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fungi support bacterial resilience following water limitation</title><author>Hestrin, Rachel ; Kan, Megan ; Lafler, Marissa ; Wollard, Jessica ; Kimbrel, Jeffrey A. ; Ray, Prasun ; Blazewicz, Steven J. ; Stuart, Rhona ; Craven, Kelly ; Firestone, Mary ; Nuccio, Erin E. ; Pett-Ridge, Jennifer</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c501t-e1afbd3f685b17c0a9985cc76a9b34d545bfec89ef760e6f2a3fceb3bcdfe2273</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>45</topic><topic>45/23</topic><topic>45/77</topic><topic>631/1647/514/1948</topic><topic>631/326/193/2539</topic><topic>631/326/2565/855</topic><topic>704/158/2165</topic><topic>704/158/2466</topic><topic>Bacteria</topic><topic>Biogeochemistry</topic><topic>Biological activity</topic><topic>Biomedical and Life Sciences</topic><topic>Community 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limitation</atitle><jtitle>The ISME Journal</jtitle><stitle>ISME J</stitle><addtitle>ISME J</addtitle><date>2022-12-01</date><risdate>2022</risdate><volume>16</volume><issue>12</issue><spage>2752</spage><epage>2762</epage><pages>2752-2762</pages><issn>1751-7362</issn><issn>1751-7370</issn><eissn>1751-7370</eissn><abstract>Drought disrupts soil microbial activity and many biogeochemical processes. Although plant-associated fungi can support plant performance and nutrient cycling during drought, their effects on nearby drought-exposed soil microbial communities are not well resolved. We used H
2
18
O quantitative stable isotope probing (qSIP) and 16S rRNA gene profiling to investigate bacterial community dynamics following water limitation in the hyphospheres of two distinct fungal lineages (
Rhizophagus irregularis
and
Serendipita bescii
) grown with the bioenergy model grass
Panicum hallii
. In uninoculated soil, a history of water limitation resulted in significantly lower bacterial growth potential and growth efficiency, as well as lower diversity in the actively growing bacterial community. In contrast, both fungal lineages had a protective effect on hyphosphere bacterial communities exposed to water limitation: bacterial growth potential, growth efficiency, and the diversity of the actively growing bacterial community were not suppressed by a history of water limitation in soils inoculated with either fungus. Despite their similar effects at the community level, the two fungal lineages did elicit different taxon-specific responses, and bacterial growth potential was greater in
R. irregularis
compared to
S. bescii
-inoculated soils. Several of the bacterial taxa that responded positively to fungal inocula belong to lineages that are considered drought susceptible. Overall, H
2
18
O qSIP highlighted treatment effects on bacterial community structure that were less pronounced using traditional 16S rRNA gene profiling. Together, these results indicate that fungal–bacterial synergies may support bacterial resilience to moisture limitation.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>36085516</pmid><doi>10.1038/s41396-022-01308-6</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0003-1315-8870</orcidid><orcidid>https://orcid.org/0000-0001-5916-9693</orcidid><orcidid>https://orcid.org/0000-0002-4439-2398</orcidid><orcidid>https://orcid.org/0000-0002-9329-2609</orcidid><orcidid>https://orcid.org/0000-0001-7517-1750</orcidid><orcidid>https://orcid.org/0000-0001-7213-9392</orcidid><orcidid>https://orcid.org/0000-0003-0189-183X</orcidid><orcidid>https://orcid.org/0000-0002-0526-0130</orcidid><orcidid>https://orcid.org/0000000172139392</orcidid><orcidid>https://orcid.org/0000000293292609</orcidid><orcidid>https://orcid.org/0000000205260130</orcidid><orcidid>https://orcid.org/000000030189183X</orcidid><orcidid>https://orcid.org/0000000244392398</orcidid><orcidid>https://orcid.org/0000000175171750</orcidid><orcidid>https://orcid.org/0000000313158870</orcidid><orcidid>https://orcid.org/0000000159169693</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 1751-7362 |
ispartof | The ISME Journal, 2022-12, Vol.16 (12), p.2752-2762 |
issn | 1751-7362 1751-7370 1751-7370 |
language | eng |
recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9666503 |
source | Oxford Journals Open Access Collection; MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central |
subjects | 45 45/23 45/77 631/1647/514/1948 631/326/193/2539 631/326/2565/855 704/158/2165 704/158/2466 Bacteria Biogeochemistry Biological activity Biomedical and Life Sciences Community structure Drought Ecology Evolutionary Biology Fungi Life Sciences Microbial activity Microbial Ecology Microbial Genetics and Genomics Microbiology Microorganisms Moisture effects Nutrient cycles Plant growth Resilience RNA, Ribosomal, 16S - genetics rRNA 16S Soil - chemistry Soil Microbiology Soil microorganisms Soil water Soils Stable isotopes Water - analysis |
title | Plant-associated fungi support bacterial resilience following water limitation |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-02T09%3A19%3A10IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Plant-associated%20fungi%20support%20bacterial%20resilience%20following%20water%20limitation&rft.jtitle=The%20ISME%20Journal&rft.au=Hestrin,%20Rachel&rft.date=2022-12-01&rft.volume=16&rft.issue=12&rft.spage=2752&rft.epage=2762&rft.pages=2752-2762&rft.issn=1751-7362&rft.eissn=1751-7370&rft_id=info:doi/10.1038/s41396-022-01308-6&rft_dat=%3Cproquest_pubme%3E2736504611%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2736504611&rft_id=info:pmid/36085516&rfr_iscdi=true |