Forfeiting the priority effect: turnover defines biofilm community succession

Colin J. Brislawn, Emily B. Graham, Karl Dana, Peter Ihardt, Sarah J. Fansler, William B. Chrisler, John B. Cliff, James C. Stegen, James J. Moran, Hans C. Bernstein

Research output: Contribution to journalArticlepeer-review

78 Scopus citations

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.

Original languageEnglish
Pages (from-to)1865-1877
Number of pages13
JournalISME Journal
Volume13
Issue number7
DOIs
StatePublished - Jul 1 2019
Externally publishedYes

Funding

Funding This work was supported by the U.S. Department of Energy (DOE), Office of Biological and Environmental Research (BER), as part of BER’s Genomic Science Program (GSP). This contribution originates from the GSP Foundational Scientific Focus Area (FSFA) at the Pacific Northwest National Laboratory (PNNL). A portion of this study was supported by PNNL’s institutional computing resource (PIC). A portion of the research was performed using EMSL, a DOE Office of Science User Facility sponsored by BER under user proposal number 49356. PNNL is operated for DOE by Battelle Memorial Institute under contract DE-AC05-76RL01830.

FundersFunder number
DOE Office of Science49356
Office of Biological and Environmental Research
U.S. Department of Energy
BattelleDE-AC05-76RL01830
Biological and Environmental Research
Pacific Northwest National Laboratory

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