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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References
Morris, J. J., Lenski, R. E. & Zinser, E. R. The Black Queen Hypothesis: evolution of dependencies through adaptive gene loss. mBio 3, e00036–12 (2012).
Cordero, O. X., Ventouras, L. A., DeLong, E. F. & Polz, M. F. Public good dynamics drive evolution of iron acquisition strategies in natural bacterioplankton populations. Proc. Natl Acad. Sci. USA 109, 20059–20064 (2012).
Lee, W., van Baalen, M. & Jansen, V. A. An evolutionary mechanism for diversity in siderophore-producing bacteria. Ecol. Lett. 15, 119–125 (2012).
Nogueira, T. et al. Horizontal gene transfer of the secretome drives the evolution of bacterial cooperation and virulence. Curr. Biol. 19, 1683–1691 (2009).
Smith, J. The social evolution of bacterial pathogenesis. Proc. Biol. Sci. 268, 61–69 (2001).
Berbee, M. L. & Taylor, J. W. Dating the molecular clock in fungi – how close are we? Fungal Biol. Rev. 24, 1–16 (2011).
Selosse, M. A. & Le Tacon, F. The land flora: a phototroph–fungus partnership? Trends Ecol. Evol. 13, 15–20 (1998).
Taylor, J. W. & Berbee, M. L. Dating divergences in the fungal tree of life: review and new analyses. Mycologia 98, 838–849 (2006).
Pirozynski, K. A. & Malloch, D. W. The origin of land plants: a matter of mycotrophism. Biosystems 5, 153–164 (1975).
Fisher, M. C. et al. Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194 (2012).
Hawksworth, D. L. The fungal dimension of biodiversity: magnitude, significance and conservation. Mycol. Res. 95, 641–655 (1991).
Hibbett, D. S. et al. A higher-level phylogenetic classification of the Fungi. Mycol. Res. 111, 509–547 (2007).
James, T. Y. et al. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443, 818–822 (2006).
Richards, T. A., Jones, M. D. M., Leonard, G. & Bass, D. Marine fungi: their ecology and molecular diversity. Annu. Rev. Mar. Sci. 4, 495–522 (2012).
Buée, M. et al. 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol. 184, 449–456 (2009).
Jumpponen, A. & Jones, K. L. Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpa phyllosphere. New Phytol. 184, 438–448 (2009).
O'brien, H. E., Parrent, J. L., Jackson, J. A., Moncalvo, J.-M. & Vilgalys, R. Fungal community analysis by large-scale sequencing of environmental samples. Appl. Environ. Microbiol. 71, 5544–5550 (2005).
Keller, N. P., Turner, G. & Bennett, J. W. Fungal secondary metabolism — from biochemistry to genomics. Nature Rev. Microbiol. 3, 937–947 (2005).
Stajich, J. E. et al. The fungi. Curr. Biol. 19, R840–R845 (2009).
Soanes, D. M. et al. Comparative genome analysis of filamentous fungi reveals gene family expansions associated with fungal pathogenesis. PLoS ONE 3, e2300 (2008).
Cornell, M. J. et al. Comparative genome analysis across a kingdom of eukaryotic organisms: specialization and diversification in the fungi. Genome Res. 17, 1809–1822 (2007).
Chiang, Y. M., Lee, K. H., Sanchez, J. F., Keller, N. P. & Wang, C. C. Unlocking fungal cryptic natural products. Nat. Prod. Commun. 4, 1505–1510 (2009).
Bushley, K. E. & Turgeon, B. G. Phylogenomics reveals subfamilies of fungal nonribosomal peptide synthetases and their evolutionary relationships. BMC Evol. Biol. 10, 26 (2010).
Amselem, J. et al. Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet. 7, e1002230 (2011).
de Boer, W., Folman, L. B., Summerbell, R. C. & Boddy, L. Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol. Rev. 29, 795–811 (2005).
Cavalier-Smith, T. in Evolutionary Biology of the Fungi (British Mycological Society Symposia) 339–353 (eds Rayer, A. D. M., Brasier, C. M. & Moore, D., 1987).
Cavalier-Smith, T. & Chao, E. E. Phylogeny and megasystematics of phagotrophic heterokonts (kingdom Chromista). J. Mol. Evol. 62, 388–420 (2006).
Bermudez Moretti, M., Perullini, A. M., Batlle, A. & Correa Garcia, S. Expression of the UGA4 gene encoding the δ-aminolevulinic and γ-aminobutyric acids permease in Saccharomyces cerevisiae is controlled by amino acid-sensing systems. Arch. Microbiol. 184, 137–140 (2005).
Boles, E. & Hollenberg, C. P. The molecular genetics of hexose transport in yeasts. FEMS Microbiol. Rev. 21, 85–111 (1997).
Heymann, P., Ernst, J. F. & Winkelmann, G. Identification of a fungal triacetylfusarinine C siderophore transport gene (TAF1) in Saccharomyces cerevisiae as a member of the major facilitator superfamily. Biometals 12, 301–306 (1999).
Gore, J., Youk, H. & van Oudenaarden, A. Snowdrift game dynamics and facultative cheating in yeast. Nature 459, 253–256 (2009).
Greig, D. & Travisano, M. The Prisoner's Dilemma and polymorphism in yeast SUC genes. Proc. Biol. Sci. 271 (Suppl. 3), S25–S26 (2004).
Crespi, B. J. The evolution of social behavior in microorganisms. Trends. Ecol. Evol. 16, 178–183 (2001).
West, S. A., Diggle, S. P., Buckling, A., Gardner, A. & Griffin, A. S. The social lives of microbes. Annu. Rev. Ecol. Evol. Syst. 38, 53–77 (2007).
Inglis, R. F., Brown, S. P. & Buckling, A. Spite versus cheats: competition among social strategies shapes virulence in Pseudomonas aeruginosa. Evolution 66, 3472–3484 (2012).
Riley, M. A. & Wertz, J. E. Bacteriocins: evolution, ecology, and application. Annu. Rev. Microbiol. 56, 117–137 (2002).
West, S. A., Griffin, A. S. & Gardner, A. Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J. Evol. Biol. 20, 415–432 (2007).
MaClean, R. C., Fuentes-Hernandez, A., Greig, D., Hurst, L. D. & Gudelj, I. A mixture of “cheats” and “co-operators” can enable maximal group benefit. PLoS Biol. 8, e1000486 (2010).
Galeote, V. et al. FSY1, a horizontally transferred gene in the Saccharomyces cerevisiae EC1118 wine yeast strain, encodes a high-affinity fructose/H+ symporter. Microbiology 156, 3754–3761 (2011).
Slot, J. C. & Hibbett, D. S. Horizontal transfer of a nitrate assimilation gene cluster and ecological transitions in fungi: a phylogenetic study. PLoS ONE 2, e1097 (2007).
Brown, C. J., Todd, K. M. & Rosenzweig, R. F. Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment. Mol. Biol. Evol. 15, 931–942 (1998).
Wei, H. et al. A putative high affinity hexose transporter, hxtA, of Aspergillus nidulans is induced in vegetative hyphae upon starvation and in ascogenous hyphae during cleistothecium formation. Fungal Genet. Biol. 41, 148–156 (2004).
Javelle, A., Andre, B., Marini, A.-M. & Chalot, M. High-affinity ammonium transporters and nitrogen sensing in mycorrhizas. Trends Microbiol. 11, 53–55 (2003).
Smith, E. E., Sims, E. H., Spencer, D. H., Kaul, R. & Olson, M. V. Evidence for diversifying selection at the pyoverdine locus of Pseudomonas aeruginosa. J. Bacteriol. 187, 2138–2147 (2005).
Kruckeberg, A. L. The hexose transporter family of Saccharomyces cerevisiae. Arch. Microbiol. 166, 283–292 (1996).
Koschwanez, J. H., Foster, K. R. & Murray, A. W. Sucrose utilization in budding yeast as a model for the origin of undifferentiated multicellularity. PLoS Biol. 9, e1001122 (2011).
Hamilton, W. D. The genetical evolution of social behaviour, I. J. Theor. Biol. 7, 1–16 (1964).
Hamilton, W. D. The genetical evolution of social behaviour, II. J. Theor. Biol. 7, 17–52 (1964).
Griffin, A. S., West, S. A. & Buckling, A. Cooperation and competition in pathogenic bacteria. Nature 430, 1024–1027 (2004).
Nadell, C. D., Foster, K. R. & Xavier, J. B. Emergence of spatial structure in cell groups and the evolution of cooperation. PLoS Comput. Biol. 6, e1000716 (2010).
Nowak, M. A. & May, R. M. Evolutionary games and spatial chaos. Nature 359, 826–829 (1992).
Hauert, C. & Doebeli, M. Spatial structure often inhibits the evolution of cooperation in the snowdrift game. Nature 428, 643–646 (2004).
Kummerli, R., Griffin, A. S., West, S. A., Buckling, A. & Harrison, F. Viscous medium promotes cooperation in the pathogenic bacterium Pseudomonas aeruginosa. Proc. Biol. Sci. 276, 3531–3538 (2009).
Kummerli, R., Gardner, A., West, S. A. & Griffin, A. S. Limited dispersal, budding dispersal, and cooperation: an experimental study. Evolution 63, 939–949 (2009).
Brockhurst, M. A., Buckling, A. & Gardner, A. Cooperation peaks at intermediate disturbance. Curr. Biol. 17, 761–765 (2007).
Verbruggen, E. et al. Spatial structure and interspecific cooperation: theory and an empirical test using the mycorrhizal mutualism. Am. Nat. 179, E133–E146 (2012).
Doolittle, W. F. Microbial evolution: stalking the wild bacterial species. Curr. Biol. 18, R565–567 (2008).
Boenigk, J., Ereshefsky, M., Hoef-Emden, K., Mallet, J. & Bass, D. Concepts in protistology: species definitions and boundaries. Eur. J. Protistol. 48, 96–102 (2012).
Taylor, J. W. et al. Phylogenetic species recognition and species concepts in fungi. Fungal Genet. Biol. 31, 21–32 (2000).
Trivers, R. L. The evolution of reciprocal altruism. Q. Rev. Biol. 46, 37–57 (1971).
Axelrod, R. & Hamilton, W. D. The evolution of cooperation. Science 211, 1390–1396 (1981).
Clutton-Brock, T. H. & Parker, G. A. Punishment in animal species. Nature 373, 209–216 (1995).
Fehr, E. & Gächter, S. Altruistic punishment in humans. Nature 415, 137–140 (2002).
Kiers, E. T. et al. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333, 880–882 (2011).
Kiers, E. T., Rousseau, R. A., West, S. A. & Denison, R. F. Host sanctions and the legume–rhizobium mutualism. Nature 425, 78–81 (2003).
Hauert, C., Holmes, M. & Doebeli, M. Evolutionary games and population dynamics: maintenance of cooperation in public goods games. Proc. Biol. Sci. 273, 2565–2570 (2006).
Archetti, M. & Scheuring, I. Coexistence of cooperation and defection in public goods games. Evolution 65, 1140–1148 (2011).
Raihani, N. J. & Bshary, R. The evolution of punishment in n-player public goods games: a volunteer's dilemma. Evolution 65, 2725–2728 (2011).
Archetti, M. et al. Economic game theory for mutualism and cooperation. Ecol. Lett. 14, 1300–1312 (2011).
Hauert, C., De Monte, S., Hofbauer, J. & Sigmund, K. Volunteering as Red Queen mechanism for cooperation in public goods games. Science 296, 1129–1132 (2002).
Floudas, D. et al. The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336, 1715–1719 (2012).
Hastrup, A. C. S. et al. Differences in crystalline cellulose modification due to degradation by brown and white rot fungi. Fungal Biol. 116, 1052–1063 (2012).
Maclean, C. R. & Brandon, C. Stable public goods cooperation and dynamic social interactions in yeast. J. Evol. Biol. 21, 1836–1843 (2008).
Garcia-Vallve, S., Romeu, A. & Palau, J. Horizontal gene transfer of glycosyl hydrolases of the rumen fungi. Mol. Biol. Evol. 17, 352–361 (2000).
Gojkovic, Z. et al. Horizontal gene transfer promoted evolution of the ability to propagate under anaerobic conditions in yeasts. Mol. Genet. Genom. 271, 387–393 (2004).
Richards, T. A., Leonard, G., Soanes, D. M. & Talbot, N. J. Gene transfer into the fungi. Fungal Biol. Rev. 25, 98–110 (2011).
Jain, R., Rivera, M. C., Moore, J. E. & Lake, J. A. Horizontal gene transfer accelerates genome innovation and evolution. Mol. Biol. Evol. 20, 1598–1602 (2003).
Gabaldon, T. & Huynen, M. A. Reconstruction of the proto-mitochondrial metabolism. Science 301, 609 (2003).
Lawrence, J. G. Microbial evolution: enforcing cooperation by partial kin selection. Curr. Biol. 19, R943–R945 (2009).
Richards, T. A., Dacks, J. B., Jenkinson, J. M., Thornton, C. R. & Talbot, N. J. Evolution of filamentous plant pathogens: gene exchange across eukaryotic kingdoms. Curr. Biol. 16, 1857–1864 (2006).
Richards, T. A. et al. Phylogenomic analysis demonstrates a pattern of rare and ancient horizontal gene transfer between plants and fungi. Plant Cell 21, 1897–1911 (2009).
Noll, K. M. & Thirangoon, K. Interdomain transfers of sugar transporters overcome barriers to gene expression. Methods Mol. Biol. 532, 309–322 (2009).
Hellborg, L., Woolfit, M., Arthursson-Hellborg, M. & Piskur, J. Complex evolution of the DAL5 transporter family. BMC Genomics 9, 164 (2008).
Gomolplitinant, K. M. & Saier, M. H. Jr. Evolution of the oligopeptide transporter family. J. Membr. Biol. 240, 89–110 (2011).
Nesbo, C. L., Nelson, K. E. & Doolittle, W. F. Suppressive subtractive hybridization detects extensive genomic diversity in Thermotoga maritima. J. Bacteriol. 184, 4475–4488 (2002).
Slot, J. C., Hallstrom, K. N., Matheny, P. B. & Hibbett, D. S. Diversification of NRT2 and the origin of its fungal homolog. Mol. Biol. Evol. 24, 1731–1743 (2007).
McDonald, T. R., Dietrich, F. S. & Lutzoni, F. Multiple horizontal gene transfers of ammonium transporters ammonia permeases from prokaryotes to eukaryotes: towards a new functional and evolutionary classification. Mol. Biol. Evol. 29, 51–60 (2012).
Coelho, M. A., Gonçalves, C., Sampaio, J. P. & Gonçalves, P. Extensive intra-kingdom horizontal gene transfer converging on a fungal fructose transporter gene. PLoS Genet. 9, e1003587 (2013).
Richards, T. A. et al. Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes. Proc. Natl Acad. Sci. USA 108, 15258–15263 (2011).
Jain, R., Rivera, M. C. & Lake, J. A. Horizontal gene transfer among genomes: the complexity hypothesis. Proc. Natl Acad. Sci. USA 96, 3801–3806 (1999).
Cohen, O., Gophna, U. & Pupko, T. The complexity hypothesis revisited: connectivity rather than function constitutes a barrier to horizontal gene transfer. Mol. Biol. Evol. 28, 1481–1489 (2011).
Uetz, P. et al. A comprehensive analysis of protein–protein interactions in Saccharomyces cerevisiae. Nature 403, 623–627 (2000).
Jeong, H., Mason, S. P., Barabasi, A. L. & Oltvai, Z. N. Lethality and centrality in protein networks. Nature 411, 41–42 (2001).
Stark, C. et al. BioGRID: a general repository for interaction datasets. Nucleic Acids Res. 34, D535–539 (2006).
Cotton, J. A. & McInerney, J. O. Eukaryotic genes of archaebacterial origin are more important than the more numerous eubacterial genes, irrespective of function. Proc. Natl Acad. Sci. USA 107, 17252–17255 (2010).
Belbahri, L., Calmin, G., Mauch, F. & Andersson, J. O. Evolution of the cutinase gene family: evidence for lateral gene transfer of a candidate Phytophthora virulence factor. Gene 408, 1–8 (2008).
de Crecy-Lagard, V., El Yacoubi, B., de la Garza, R. D., Noiriel, A. & Hanson, A. D. Comparative genomics of bacterial and plant folate synthesis and salvage: predictions and validations. BMC Genomics 8, 245 (2007).
Lehmann, L., Bargum, K. & Reuter, M. An evolutionary analysis of the relationship between spite and altruism. J. Evol. Biol. 19, 1507–1516 (2006).
Harrison, F. & Buckling, A. Siderophore production and biofilm formation as linked social traits. ISME J. 3, 632–634 (2009).
Williams, P., Winzer, K., Chan, W. C. & Camara, M. Look who's talking: communication and quorum sensing in the bacterial world. Phil. Trans. R. Soc. B 362, 1119–1134 (2007).
Fox, E. M. & Howlett, B. J. Secondary metabolism: regulation and role in fungal biology. Curr. Opin. Microbiol. 11, 481–487 (2008).
Trejo-Estrada, S. R., Paszczynski, A. & Crawford, D. L. Antibiotics and enzymes produced by the biocontrol agent Streptomyces violaceusniger YCED-9. J. Ind. Microbiol. Biotechnol. 21, 81–90 (1998).
Friesen, T. L. et al. Emergence of a new disease as a result of interspecific virulence gene transfer. Nature Genet. 38, 953–956 (2006).
Patron, N. J. et al. Origin and distribution of epipolythiodioxopiperazine (ETP) gene clusters in filamentous ascomycetes. BMC Evol. Biol. 7, 174 (2007).
Slot, J. C. & Rokas, A. Horizontal transfer of a large and highly toxic secondary metabolic gene cluster between fungi. Curr. Biol. 21, 134–139 (2011).
Powell, M. J., Letcher, P. M. & Longcore, J. E. Pseudorhizidium is a new genus with distinct zoospore ultrastructure in the order Chytridiales. Mycologia 105, 496–507 (2013).
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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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)
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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DOI: https://doi.org/10.1038/nrmicro3108
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