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. 2020 Feb 18;117(7):3656-3662.
doi: 10.1073/pnas.1917265117. Epub 2020 Feb 3.

Ecological drivers of bacterial community assembly in synthetic phycospheres

He Fu  1 , Mario Uchimiya  1   2 , Jeff Gore  3 , Mary Ann Moran  4
Affiliations

Ecological drivers of bacterial community assembly in synthetic phycospheres

He Fu et al. Proc Natl Acad Sci U S A. .

Abstract

In the nutrient-rich region surrounding marine phytoplankton cells, heterotrophic bacterioplankton transform a major fraction of recently fixed carbon through the uptake and catabolism of phytoplankton metabolites. We sought to understand the rules by which marine bacterial communities assemble in these nutrient-enhanced phycospheres, specifically addressing the role of host resources in driving community coalescence. Synthetic systems with varying combinations of known exometabolites of marine phytoplankton were inoculated with seawater bacterial assemblages, and communities were transferred daily to mimic the average duration of natural phycospheres. We found that bacterial community assembly was predictable from linear combinations of the taxa maintained on each individual metabolite in the mixture, weighted for the growth each supported. Deviations from this simple additive resource model were observed but also attributed to resource-based factors via enhanced bacterial growth when host metabolites were available concurrently. The ability of photosynthetic hosts to shape bacterial associates through excreted metabolites represents a mechanism by which microbiomes with beneficial effects on host growth could be recruited. In the surface ocean, resource-based assembly of host-associated communities may underpin the evolution and maintenance of microbial interactions and determine the fate of a substantial portion of Earth's primary production.

Keywords: community assembly; phycospheres; phytoplankton–bacteria interactions.

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Conflict of interest statement

The authors declare no competing interest.

Figures

Fig. 1.
Fig. 1.
Experimental design of the synthetic phycospheres. (A) Ten metabolites characteristic of diatom or dinoflagellate phycospheres were identified from differential gene expression by a reporter bacterium, R. pomeroyi DSS-3, in a coculture dominated by a dinoflagellate (A. tamarense) for the first 12 d (time points 1, 2, and 3) and by a diatom (T. pseudonana) for the final 15 d (time points 6, 7, and 8). Data from ref. . (B) The 96-well plates contained 22 media types containing combinations of diatom metabolites or dinoflagellate metabolites, with each medium replicated four times. Following inoculation with a natural bacterial community from coastal seawater, communities were transferred daily and analyzed by 16S rRNA sequencing after eight growth-dilution cycles (P8). The composition of mixed-resource media A1 through A6 and B1 through B6 is shown in the upper matrix, where an empty dot signifies the absence of a metabolite.
Fig. 2.
Fig. 2.
Composition of bacterial communities in the P8 growth cycle of diatom phycospheres (Left), dinoflagellate phycospheres (Right), and the inoculum (Center) based on 97% identity OTUs of 16S rRNA amplicons. Gray coloring indicates OTUs that made up <0.1% of the pooled final bacterial communities. OTU0001 made up 0.4% of the inoculum community.
Fig. 3.
Fig. 3.
Observed versus predicted OTU percent abundance in mixed-resource phycosphere communities. Dotted line and shading, linear regression and 95% CI of observed versus predicted based on a WS null model; solid line, 1:1 relationship between observed and predicted. (Left) Data from media A1 and B1 (five metabolite mixtures); only OTUs accounting for ≥ 1% of the community are shown for simplicity. (Right) Data from media A2 through A6 and B2 through B6 (four metabolite mixtures); only OTU0001 is plotted for simplicity (see SI Appendix, Fig. S5 for complete plots). Red stars indicate significant overrepresentation of OTUs in the mixed-resource communities. Error bars indicate ±1 SE.
Fig. 4.
Fig. 4.
Observed versus predicted OD600 of R. pomeroyi DSS-3 after eight growth-dilution cycles in mixed-resource phycospheres. Blue symbols indicate diatom media (A1 through A6) and green symbols indicate dinoflagellate media (B1 through B6). Dotted lines, linear regression; solid line, 1:1 relationship between observed and predicted. Error bars (± 1 SE) all fall within the symbols. Light blue symbols mark the metabolite mixtures (A5 and A6) for which observed OD600 fell within the 95% CI of the predicted OD600.
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