Forfeiting the priority effect: turnover defines biofilm community succession
Microbial community succession is a fundamental process that affects underlying functions of almost all ecosystems; yet the roles and fates of the most abundant colonizers are often poorly understood. Does early abundance spur long term persistence? How do deterministic and stochastic processes infl...
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Published in | The ISME Journal Vol. 13; no. 7; pp. 1865 - 1877 |
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Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
London
Nature Publishing Group UK
01.07.2019
Oxford University Press Springer Nature |
Subjects | |
Online Access | Get full text |
ISSN | 1751-7362 1751-7370 1751-7370 |
DOI | 10.1038/s41396-019-0396-x |
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Abstract | Microbial community succession is a fundamental process that affects underlying functions of almost all ecosystems; yet the roles and fates of the most abundant colonizers are often poorly understood. Does early abundance spur long term persistence? How do deterministic and stochastic processes influence the ecological contribution of colonizers? We performed a succession experiment within a hypersaline ecosystem to investigate how different processes contributed to the turnover of founder species. Bacterial and eukaryotic colonizers were identified during primary succession and tracked through a defined, 79-day biofilm maturation period using 16S and 18S rRNA gene sequencing in combination with high resolution imaging that utilized stable isotope tracers to evaluate successional patterns of primary producers and nitrogen fixers. The majority of the founder species did not maintain high abundance throughout succession. Species replacement (versus loss) was the dominant process shaping community succession. We also asked if different ecological processes acted on bacteria versus Eukaryotes during succession and found deterministic and stochastic forces corresponded more with microeukaryote and bacterial colonization, respectively. Our results show that taxa and functions belonging to different kingdoms, which share habitat in the tight spatial confines of a biofilm, were influenced by different ecological processes and time scales of succession. |
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AbstractList | Microbial community succession is a fundamental process that affects underlying functions of almost all ecosystems; yet the roles and fates of the most abundant colonizers are often poorly understood. Does early abundance spur long term persistence? How do deterministic and stochastic processes influence the ecological contribution of colonizers? We performed a succession experiment within a hypersaline ecosystem to investigate how different processes contributed to the turnover of founder species. Bacterial and eukaryotic colonizers were identified during primary succession and tracked through a defined, 79-day biofilm maturation period using 16S and 18S rRNA gene sequencing in combination with high resolution imaging that utilized stable isotope tracers to evaluate successional patterns of primary producers and nitrogen fixers. The majority of the founder species did not maintain high abundance throughout succession. Species replacement (versus loss) was the dominant process shaping community succession. We also asked if different ecological processes acted on bacteria versus Eukaryotes during succession and found deterministic and stochastic forces corresponded more with microeukaryote and bacterial colonization, respectively. Our results show that taxa and functions belonging to different kingdoms, which share habitat in the tight spatial confines of a biofilm, were influenced by different ecological processes and time scales of succession. Microbial community succession is a fundamental process that affects underlying functions of almost all ecosystems; yet the roles and fates of the most abundant colonizers are often poorly understood. Does early abundance spur long term persistence? How do deterministic and stochastic processes influence the ecological contribution of colonizers? We performed a succession experiment within a hypersaline ecosystem to investigate how different processes contributed to the turnover of founder species. Bacterial and eukaryotic colonizers were identified during primary succession and tracked through a defined, 79-day biofilm maturation period using 16S and 18S rRNA gene sequencing in combination with high resolution imaging that utilized stable isotope tracers to evaluate successional patterns of primary producers and nitrogen fixers. The majority of the founder species did not maintain high abundance throughout succession. Species replacement (versus loss) was the dominant process shaping community succession. We also asked if different ecological processes acted on bacteria versus Eukaryotes during succession and found deterministic and stochastic forces corresponded more with microeukaryote and bacterial colonization, respectively. Our results show that taxa and functions belonging to different kingdoms, which share habitat in the tight spatial confines of a biofilm, were influenced by different ecological processes and time scales of succession.Microbial community succession is a fundamental process that affects underlying functions of almost all ecosystems; yet the roles and fates of the most abundant colonizers are often poorly understood. Does early abundance spur long term persistence? How do deterministic and stochastic processes influence the ecological contribution of colonizers? We performed a succession experiment within a hypersaline ecosystem to investigate how different processes contributed to the turnover of founder species. Bacterial and eukaryotic colonizers were identified during primary succession and tracked through a defined, 79-day biofilm maturation period using 16S and 18S rRNA gene sequencing in combination with high resolution imaging that utilized stable isotope tracers to evaluate successional patterns of primary producers and nitrogen fixers. The majority of the founder species did not maintain high abundance throughout succession. Species replacement (versus loss) was the dominant process shaping community succession. We also asked if different ecological processes acted on bacteria versus Eukaryotes during succession and found deterministic and stochastic forces corresponded more with microeukaryote and bacterial colonization, respectively. Our results show that taxa and functions belonging to different kingdoms, which share habitat in the tight spatial confines of a biofilm, were influenced by different ecological processes and time scales of succession. |
Author | Cliff, John B. Brislawn, Colin J. Ihardt, Peter Fansler, Sarah J. Stegen, James C. Graham, Emily B. Moran, James J. Dana, Karl Bernstein, Hans C. Chrisler, William B. |
Author_xml | – sequence: 1 givenname: Colin J. surname: Brislawn fullname: Brislawn, Colin J. organization: Biological Sciences Division, Pacific Northwest National Laboratory – sequence: 2 givenname: Emily B. orcidid: 0000-0002-4623-7076 surname: Graham fullname: Graham, Emily B. organization: Biological Sciences Division, Pacific Northwest National Laboratory – sequence: 3 givenname: Karl surname: Dana fullname: Dana, Karl organization: Signature Science and Technology Division, Pacific Northwest National Laboratory – sequence: 4 givenname: Peter surname: Ihardt fullname: Ihardt, Peter organization: Signature Science and Technology Division, Pacific Northwest National Laboratory – sequence: 5 givenname: Sarah J. orcidid: 0000-0003-4190-907X surname: Fansler fullname: Fansler, Sarah J. organization: Biological Sciences Division, Pacific Northwest National Laboratory – sequence: 6 givenname: William B. surname: Chrisler fullname: Chrisler, William B. organization: Biological Sciences Division, Pacific Northwest National Laboratory, Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory – sequence: 7 givenname: John B. surname: Cliff fullname: Cliff, John B. organization: Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory – sequence: 8 givenname: James C. orcidid: 0000-0001-9135-7424 surname: Stegen fullname: Stegen, James C. organization: Biological Sciences Division, Pacific Northwest National Laboratory – sequence: 9 givenname: James J. surname: Moran fullname: Moran, James J. email: James.Moran@pnnl.gov organization: Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory – sequence: 10 givenname: Hans C. orcidid: 0000-0003-2913-7708 surname: Bernstein fullname: Bernstein, Hans C. email: Hans.C.Bernstein@uit.no organization: Faculty of Biosciences, Fisheries and Economics, UiT - The Arctic University of Norway, The Arctic Centre for Sustainable Energy, UiT - The Arctic University of Norway |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30886318$$D View this record in MEDLINE/PubMed |
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Title | Forfeiting the priority effect: turnover defines biofilm community succession |
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