Bacterial–fungal interactions revealed by genome-wide analysis of bacterial mutant fitness

Emily C. Pierce, Manon Morin, Jessica C. Little, Roland B. Liu, Joanna Tannous, Nancy P. Keller, Kit Pogliano, Benjamin E. Wolfe, Laura M. Sanchez, Rachel J. Dutton

Research output: Contribution to journalArticlepeer-review

81 Scopus citations

Abstract

Microbial interactions are expected to be major determinants of microbiome structure and function. Although fungi are found in diverse microbiomes, their interactions with bacteria remain largely uncharacterized. In this work, we characterize interactions in 16 different bacterial–fungal pairs, examining the impacts of 8 different fungi isolated from cheese rind microbiomes on 2 bacteria (Escherichia coli and a cheese-isolated Pseudomonas psychrophila). Using random barcode transposon-site sequencing with an analysis pipeline that allows statistical comparisons between different conditions, we observed that fungal partners caused widespread changes in the fitness of bacterial mutants compared to growth alone. We found that all fungal species modulated the availability of iron and biotin to bacterial species, which suggests that these may be conserved drivers of bacterial–fungal interactions. Species-specific interactions were also uncovered, a subset of which suggested fungal antibiotic production. Changes in both conserved and species-specific interactions resulted from the deletion of a global regulator of fungal specialized metabolite production. This work highlights the potential for broad impacts of fungi on bacterial species within microbiomes.

Original languageEnglish
Pages (from-to)87-102
Number of pages16
JournalNature Microbiology
Volume6
Issue number1
DOIs
StatePublished - Jan 2021
Externally publishedYes

Funding

The authors would like to thank the following people and groups: the Arkin Lab and the Deutschbauer Lab at UC Berkeley for the E. coli Keio_ML9 RB-TnSeq library; K. Jepsen at the IGM Genomics Center at the University of California, San Diego for assistance with sequencing; S. Kryazhimskiy (UCSD) for his input on RB-TnSeq data processing; C. Dinh (UCSD) for assistance with fungal genome assembly; W. Bushnell (UCSD) for assistance with fitness validation experiments; S. Beyhan (JCVI) for advice on fungal genome annotation; L. Marotz (UCSD) for assistance with non-cheese yeasts; and members of the Dutton Lab, especially B. Anderson and C. Saak, for constructive comments on the manuscript. This work was supported by the National Institutes of Health grant nos. T32-AT007533 (to J.C.L.) and F31-AT010418 (to J.C.L.), the National Institutes of Health grant no. R01-AI117712 (to R.B.L), National Science Foundation grant no. MCB-1817955 (to L.M.S.), National Science Foundation grant no. MCB-1817887 (to R.J.D. and L.M.S.), National Science Foundation grant no. MCB-1715553 (to B.E.W.), the UCSD Center for Microbiome Innovation (to E.C.P.), the UCSD Ruth Stern Award (to E.C.P.), NIH Institutional Training grant no. 5 T32 GM 7240-40 (to E.C.P.) and the National Institutes of Health grant no. R01GM112739-01 (to N.P.K.).

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