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Horizontal gene transfer in osmotrophs: playing with public goods

Abstract

Osmotrophic microorganisms, such as fungi and oomycetes, feed by secreting depolymerizing enzymes to process complex food sources in the extracellular environment, and taking up the resulting simple sugars, micronutrients and amino acids. As a consequence of this lifestyle, osmotrophs engage in the acquisition and protection of public goods. In this Opinion article, we propose that horizontal gene transfer (HGT) has played a key part in shaping both the repertoire of proteins required for osmotrophy and the nature of public goods interactions in which eukaryotic microorganisms engage.

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Figure 1: The osmotrophic lifestyle in eukaryotic microorganisms.
Figure 2: Competitors and collaborators in an osmotrophic ecosystem.
Figure 3: Comparison of protein–protein interaction conmplexity between horizontally transferred genes and osmotrophic genes in the Saccharomyces cerevisiae S288c genome.

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Acknowledgements

T.A.R. is a European Molecular Biology Organization Young Investigator and a Leverhulme Early Career Fellow, and his research group is supported by grants from the Moore Foundation, the UK Natural Environment Research Council and the Biotechnology and Biological Sciences Research Council (BBSRC). N.J.T. is a European Research Council Advanced Investigator and receives funding from the BBSRC, the Bill and Melinda Gates Foundation and the Halpin Trust. The authors thank A. Buckling and the anonymous reviewers for comments on this manuscript.

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Correspondence to Nicholas J. Talbot.

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Supplementary information

Supplementary information S1 (table)

Horizontal gene transfer of secreted degradative enzymes. (PDF 236 kb)

Supplementary information S2 (table)

Horizontal gene transfer of metabolite uptake transporters. (PDF 216 kb)

Supplementary information S3 (table)

Horizontal gene transfer of toxin production and/or detoxification (gene clusters are signified by multiple accession number per transfer). (PDF 234 kb)

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Glossary

Appressoria

Specialized infection cells that are used by plant-pathogenic fungi to penetrate the host plant surface using mechanical force and/or enzymatic action to breach the cuticle.

Cheats

Individuals within a community that do not carry out cooperative behaviours (or that minimize their cooperation) but derive benefit from the work of others.

Club goods

Public goods that are accessible to select individuals only ('members of the club') in the community.

Cooperators

Individuals that provide benefit to others.

Haustoria

Specialized fungal feeding structures that are commonly produced by biotrophic fungi and occupy living plant cells by invagination of the plant plasma membrane.

Horizontal gene transfer

The transfer of genetic material between genomes (for example, across species boundaries). Also called lateral gene transfer.

Hyphae

Cells of a filamentous morphotype, sometimes forming branching structures; this morphotype exists for fungi and some other microorganisms. The development of this cellular morphology is governed by the cytoskeleton, with growth and trophic activity directed to the hyphal tip.

Inclusive fitness

The result of individual behaviours on the reproductive output of others, weighted by relatedness.

Kin selection

Selection that favours traits because of their beneficial effects on the fitness of relatives.

Osmotrophic microorganisms

Microorganisms that take up digested or dissolved nutrients by osmosis, often facilitated by transporter proteins to allow molecules to cross the cell membrane.

Phagotrophy

A process governed by the cytoskeleton and involving membrane and cytoplasmic manipulation to engulf large particles or other cells for nutrition.

Private goods

Biological or chemical resources that are produced by an individual and can be used only by that individual.

Public goods

Biological or chemical resources that are produced by an individual in a community and can be used by all other individuals in the community.

Relatedness

A measure of genetic or genomic similarity.

Rhizoid structures

'Hair-like' protruberances of eukaryotic cells that maximize the interface between the cell surface and the environment.

Siderophores

Small-molecule iron-chelating compounds that are secreted by microorganisms.

Spiteful behaviour

Behaviour that is costly to both the producer and the recipient.

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Richards, T., Talbot, N. Horizontal gene transfer in osmotrophs: playing with public goods. Nat Rev Microbiol 11, 720–727 (2013). https://doi.org/10.1038/nrmicro3108

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