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Horizontal Gene Transfer in Osmotrophs: Playing with Public Goods

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Horizontal Gene Transfer in Osmotrophs: Playing with Public Goods ORE Open Research Exeter TITLE Horizontal gene transfer in osmotrophs: playing with public goods. AUTHORS Richards, Thomas A; Talbot, Nicholas J. JOURNAL Nat Rev Microbiol DEPOSITED IN ORE 19 November 2014 This version available at http://hdl.handle.net/10871/15898 COPYRIGHT AND REUSE Open Research Exeter makes this work available in accordance with publisher policies. A NOTE ON VERSIONS The version presented here may differ from the published version. If citing, you are advised to consult the published version for pagination, volume/issue and date of publication PERSPECTIVES however, not unique to fungi. Many bacteria, OPINION for instance, feed in an analogous man­ ner, and other eukaryotic groups, such as Horizontal gene transfer in hypho­chytriomycetes (FIG. 1c) and oomycetes (FIG. 1d) (sometimes collectively termed the pseudofungi26), also feed osmotrophically osmotrophs: playing with public and adopt filamentous growth habits, allow­ ing invasive growth in heterogeneous sub­ goods strates. Importantly, these eukaryotes also lost the ability to carry out phagotrophy and Thomas A. Richards and Nicholas J. Talbot became obligately osmotrophic26,27. Osmotrophy has a number of distinct Abstract | Osmotrophic microorganisms, such as fungi and oomycetes, feed advantages as a feeding strategy. External by secreting depolymerizing enzymes to process complex food sources in the digestion of large and complex polymers extracellular environment, and taking up the resulting simple sugars, micronutrients allows greater control over substances that and amino acids. As a consequence of this lifestyle, osmotrophs engage in the are allowed to enter a cell (FIG. 2a), thus acquisition and protection of public goods. In this Opinion article, we propose that minimizing potential routes of infection and intake of harmful substances. Furthermore, horizontal gene transfer (HGT) has played a key part in shaping both the repertoire osmotrophy allows greater fidelity in nutri­ of proteins required for osmotrophy and the nature of public goods interactions in ent acquisition, such that the repertoire of which eukaryotic microorganisms engage. digestive enzymes and uptake transporters expressed by an osmotrophic species can Osmotrophic microorganisms feed by secret­ the fossil record, fungi colonized the ter­ be altered to match a particular need, like ing extracellular depolymerizing enzymes restrial environ­ment more than 400 million the colonization of a new substrate28–30. into the environment to degrade complex years ago, in close association with early However, osmotrophy also carries some polymers, such as cellulose, lignin and land plants6–9. Extant fungi occupy diverse disadvantages or risks, such as the utilization proteins, and by transporting the resulting ecosystems and undertake a wide variety of secreted enzymes by competitors within a simple, monomeric sugars and amino acids of interactions, ranging from highly mutu­ community and the loss of derived nutrient into their own cells. Fungi, oomycetes and alistic symbioses to devastating diseases of sources to neighbouring microorganisms many bacteria feed by osmotrophy, and in both animals and plants10. Fungi are diverse (FIG. 2b,c) or by diffusion30–32. An important using this trophic mechanism, these organ­ in terms of species complexity11–17, gene consequence of osmotrophy is therefore isms have become the principal degraders repertoire and biochemical capabilities18–24, that microorganisms which use this trophic of biomass in most terrestrial ecosystems, as and form a range of cell types, including mechanism must engage in producing, well as important pathogens of plants and uni­cellular yeasts, motile flagellated zoo­ protecting and acquiring public goods33,34. animals. One of the most important conse­ spores and polarized multicellular hyphae. Thus, osmotrophy-associated genes pre­ quences of osmotrophy is the participation They also form specialized feeding struc­ dominantly encode secreted depolymerizing of microorganisms in both competitive tures, such as appressoria (FIG. 1a), haustoria enzymes and cognate transporter proteins and cooperative public goods interactions, and rhizoid structures (FIG. 1b), which can go (FIG. 2), as well as genes associated with toxin because the food sources of these organ­ on to form complex tissues within multi­ production or detoxification. Toxin produc­ isms reside outside the cells even as these cellular fruiting bodies12. It is clear that tion can be used by osmotrophs to exclude foods are being processed, and are therefore early in the diversification of fungi, the competitors, thereby protecting public goods available to others. In this Opinion article, ability to carry out phagocytosis — a mode from being used by others (for examples, see we focus primarily on microbial eukaryotes of feeding that generates private goods — REFS 35,36). The acquisition or reconfigura­ and propose that genes encoding proteins was lost, and the overwhelming majority tion of these traits is likely to be favourable, associated with osmotrophy have been of extant fungi are instead dependent on as both allow microorganisms to colonize important in the evolutionary ecology and osmotrophy13, a process that generates both new environments and/or make use of addi­ public goods interactions of these micro­ public and club goods. tional metabolites, but also equip microor­ organisms. We also present evidence that Osmotrophy has proved to be a success­ ganisms with new capabilities with which to horizontal gene transfer (HGT) has had a ful feeding strategy for fungi in particular, engage in social competition (for example, major role in reconfiguring osmotrophic and has allowed them to colonize diverse stealing bacterial siderophores30). functions in fungi and oomycetes. These heterogeneous terrestrial environments results are part of a growing body of evi­ where nutrients are plentiful but largely Osmotrophs and public goods interactions dence which suggests that diverse evolution­ inaccessible to most competitors because As discussed above, the production of ary mechanisms operating on genomes have they take the form of complex biological osmotrophic phenotypes represents a cost shaped social interactions across a range of molecules such as cellulose and lignin (for to the individual, because a fraction of the microorganisms1–5. example, within leaf litter or soil) or the cel­ protein produced or food digested might be lulose- and protein-rich tissues of plant and lost to competitors32,34. As a result, selection Osmotrophic eukaryotic microorganisms animal hosts, respectively. As a consequence, will tend to favour individuals that stop or The largest group of osmotrophic eukary­ fungi have evolved to become important minimize their production of public goods otic microorganisms, in terms of biodiver­ decomposers of biomass in most terres­ but still make use of public goods manu­ sity, is the kingdom Fungi. According to trial ecosystems25. Obligate osmotrophy is, factured by others. Cooperative behaviour 720 | OCTOBER 2013 | VOLUME 11 www.nature.com/reviews/micro © 2013 Macmillan Publishers Limited. All rights reserved PERSPECTIVES 31 a b and glucose outside the cell , where a suite of hexose transporters are then utilized to recover extracellular sugars29,41,45. This osmo­ trophic process can result in the loss (into the environment) of up to 99% of the mono­ saccharides produced by invertase activity31 (but see REF. 46 for a scenario suggesting that this 99% is not all lost). The production of extracellular enzymes such as invertase clearly carries a cost to the organism, and it is therefore likely that selection favours indi­ viduals which have lost their invertase activity but still survive as cheats in a population of c d invertase secretors (a scenario analogous to that set out in the Black Queen hypothesis1). Alternatively, acquisition of activities such as invertase production might confer on a microbial lineage the ability to colonize new environments and utilize previously untapped food sources. Complex patterns of gain and loss of the genes encoding secreted depolymerizing enzymes and cognate nutri­ ent uptake transporters are thus likely to occur within osmotrophic lineages. It is Figure 1 | The osmotrophic lifestyle in eukaryotic microorganisms. a | Scanning electron micro- therefore clear to see how a process such as graph (SEM) of Magnaporthe oryzae, showing appressoria, which areNature specialized Reviews structures | Microbiology for the HGT might provide a means for such traits invasion of plant tissue. b | Light micrograph of sporangia and rhizoid structures of Pseudorhizidium to rapidly move within a population of endosporangiatum (isolate JEL 221)106. c | SEM of a fraction of a clonal multicellular assembly (or myce- different species. lium) of the pseudofungus Hyphochytrium catenoides, showing hyphal growth and interconnections. d | SEM of Phytophthora infestans attacking the leaf surface of a host plant. Scale bars represent 10 μm. Osmotrophic and social evolution Part b image courtesy of J. Longcore, University of Maine, USA; part d image courtesy of S. Kamoun, There have been considerable advances The Sainsbury Laboratory, UK. in our understanding of social inter­ actions in microbial systems (for reviews, see REFS 33,34). These interactions have can therefore give way to the emergence of — those organisms that possess a compat­ been interpreted mainly using classic cheats within a population34,37. It is generally ible uptake system (a cognate
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