Horizontal gene transfer in osmotrophs: Playing with public goods

Nature Reviews Microbiology

Volumn 11, Issue 10, 2013, Pages 720-727

  Richards, Thomas A ^a,b   Talbot, Nicholas J ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; MICROBIAL ENZYME; SUGAR; TRACE ELEMENT;

ENZYME RELEASE; EUKARYOTE; GENE TRANSFER; MICROBIAL METABOLISM; MICROORGANISM; NONHUMAN; OSMOTROPHIC MICROORGANISM; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW;

CARBOHYDRATE METABOLISM; ENVIRONMENT; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; GENE TRANSFER, HORIZONTAL; GENES, FUNGAL; OOMYCETES; PHENOTYPE; PHYLOGENY; PROTEIN INTERACTION MAPPING; SACCHAROMYCES CEREVISIAE; SPECIES SPECIFICITY; SYMBIOSIS;

EUKARYOTA; FUNGI; OOMYCETES;

EID: 84884282697     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro3108     Document Type: Review

References (106)

1. 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).
2. 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).
3. Lee, W., van Baalen, M. & Jansen, V. A. An evolutionary mechanism for diversity in siderophore-producing bacteria. Ecol. Lett. 15, 119-125 (2012).
4. Nogueira, T. et al. Horizontal gene transfer of the secretome drives the evolution of bacterial cooperation and virulence. Curr. Biol. 19, 1683-1691 (2009).
5. Smith, J. The social evolution of bacterial pathogenesis. Proc. Biol. Sci. 268, 61-69 (2001). (Pubitemid 32127954)
6. Berbee, M. L. & Taylor, J. W. Dating the molecular clock in fungi - how close are we? Fungal Biol. Rev. 24, 1-16 (2011).
7. Selosse, M. A. & Le Tacon, F. The land flora: a phototroph-fungus partnership? Trends Ecol. Evol. 13, 15-20 (1998).
8. Taylor, J. W. & Berbee, M. L. Dating divergences in the fungal tree of life: review and new analyses. Mycologia 98, 838-849 (2006). (Pubitemid 46683208)
9. Pirozynski, K. A. & Malloch, D. W. The origin of land plants: a matter of mycotrophism. Biosystems 5, 153-164 (1975).
10. Fisher, M. C. et al. Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186-194 (2012).
11. Hawksworth, D. L. The fungal dimension of biodiversity: magnitude, significance and conservation. Mycol. Res. 95, 641-655 (1991).
12. Hibbett, D. S. et al. A higher-level phylogenetic classification of the Fungi. Mycol. Res. 111, 509-547 (2007). (Pubitemid 46915419)
13. James, T. Y. et al. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443, 818-822 (2006). (Pubitemid 44622687)
14. 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).
15. Buée, M. et al. 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol. 184, 449-456 (2009).
16. Jumpponen, A. & Jones, K. L. Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpa phyllosphere. New Phytol. 184, 438-448 (2009).
17. 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). (Pubitemid 41338289)
18. Keller, N. P., Turner, G. & Bennett, J. W. Fungal secondary metabolism - from biochemistry to genomics. Nature Rev. Microbiol. 3, 937-947 (2005). (Pubitemid 43078157)
19. Stajich, J. E. et al. The fungi. Curr. Biol. 19, R840-R845 (2009).
20. Soanes, D. M. et al. Comparative genome analysis of filamentous fungi reveals gene family expansions associated with fungal pathogenesis. PLoS ONE 3, e2300 (2008).
21. 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). (Pubitemid 351360005)
22. 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).
23. Bushley, K. E. & Turgeon, B. G. Phylogenomics reveals subfamilies of fungal nonribosomal peptide synthetases and their evolutionary relationships. BMC Evol. Biol. 10, 26 (2010).
24. Amselem, J. et al. Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet. 7, e1002230 (2011).
25. 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). (Pubitemid 41139182)
26. 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).
27. Cavalier-Smith, T. & Chao, E. E. Phylogeny and megasystematics of phagotrophic heterokonts (kingdom Chromista). J. Mol. Evol. 62, 388-420 (2006).
28. 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). (Pubitemid 41504139)
29. Boles, E. & Hollenberg, C. P. The molecular genetics of hexose transport in yeasts. FEMS Microbiol. Rev. 21, 85-111 (1997). (Pubitemid 27376760)
30. 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). (Pubitemid 30139281)
31. Gore, J., Youk, H. & van Oudenaarden, A. Snowdrift game dynamics and facultative cheating in yeast. Nature 459, 253-256 (2009).
32. Greig, D. & Travisano, M. The Prisoner's Dilemma and polymorphism in yeast SUC genes. Proc. Biol. Sci. 271 (Suppl. 3), S25-S26 (2004). (Pubitemid 38186899)
33. Crespi, B. J. The evolution of social behavior in microorganisms. Trends. Ecol. Evol. 16, 178-183 (2001). (Pubitemid 32197564)
34. 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).
35. 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).
36. Riley, M. A. & Wertz, J. E. Bacteriocins: evolution, ecology, and application. Annu. Rev. Microbiol. 56, 117-137 (2002). (Pubitemid 35217450)
37. 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).
38. 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).
39. 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).
40. 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).
41. 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). (Pubitemid 28364447)
42. 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). (Pubitemid 38058449)
43. Javelle, A., Andre, B., Marini, A.-M. & Chalot, M. High-affinity ammonium transporters and nitrogen sensing in mycorrhizas. Trends Microbiol. 11, 53-55 (2003). (Pubitemid 36207496)
44. 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). (Pubitemid 40316244)
45. Kruckeberg, A. L. The hexose transporter family of Saccharomyces cerevisiae. Arch. Microbiol. 166, 283-292 (1996). (Pubitemid 26400530)
46. 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).
47. Hamilton, W. D. The genetical evolution of social behaviour, I. J. Theor. Biol. 7, 1-16 (1964).
48. Hamilton, W. D. The genetical evolution of social behaviour, II. J. Theor. Biol. 7, 17-52 (1964).
49. Griffin, A. S., West, S. A. & Buckling, A. Cooperation and competition in pathogenic bacteria. Nature 430, 1024-1027 (2004). (Pubitemid 39128386)
50. 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).
51. Nowak, M. A. & May, R. M. Evolutionary games and spatial chaos. Nature 359, 826-829 (1992). (Pubitemid 23398292)
52. Hauert, C. & Doebeli, M. Spatial structure often inhibits the evolution of cooperation in the snowdrift game. Nature 428, 643-646 (2004). (Pubitemid 38524804)
53. 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).
54. Kummerli, R., Gardner, A., West, S. A. & Griffin, A. S. Limited dispersal, budding dispersal, and cooperation: an experimental study. Evolution 63, 939-949 (2009).
55. Brockhurst, M. A., Buckling, A. & Gardner, A. Cooperation peaks at intermediate disturbance. Curr. Biol. 17, 761-765 (2007). (Pubitemid 46635105)
56. Verbruggen, E. et al. Spatial structure and interspecific cooperation: theory and an empirical test using the mycorrhizal mutualism. Am. Nat. 179, E133-E146 (2012).
57. Doolittle, W. F. Microbial evolution: stalking the wild bacterial species. Curr. Biol. 18, R565-567 (2008). (Pubitemid 351888932)
58. 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).
59. Taylor, J. W. et al. Phylogenetic species recognition and species concepts in fungi. Fungal Genet. Biol. 31, 21-32 (2000). (Pubitemid 32066164)
60. Trivers, R. L. The evolution of reciprocal altruism. Q. Rev. Biol. 46, 37-57 (1971).
61. Axelrod, R. & Hamilton, W. D. The evolution of cooperation. Science 211, 1390-1396 (1981). (Pubitemid 11107890)
62. Clutton-Brock, T. H. & Parker, G. A. Punishment in animal species. Nature 373, 209-216 (1995).
63. Fehr, E. & Gächter, S. Altruistic punishment in humans. Nature 415, 137-140 (2002). (Pubitemid 34059509)
64. Kiers, E. T. et al. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333, 880-882 (2011).
65. Kiers, E. T., Rousseau, R. A., West, S. A. & Denison, R. F. Host sanctions and the legume- rhizobium mutualism. Nature 425, 78-81 (2003). (Pubitemid 37101720)
66. 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). (Pubitemid 44439679)
67. Archetti, M. & Scheuring, I. Coexistence of cooperation and defection in public goods games. Evolution 65, 1140-1148 (2011).
68. Raihani, N. J. & Bshary, R. The evolution of punishment in n-player public goods games: a volunteer's dilemma. Evolution 65, 2725-2728 (2011).
69. Archetti, M. et al. Economic game theory for mutualism and cooperation. Ecol. Lett. 14, 1300-1312 (2011).
70. 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). (Pubitemid 34517132)
71. Floudas, D. et al. The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336, 1715-1719 (2012).
72. 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).
73. Maclean, C. R. & Brandon, C. Stable public goods cooperation and dynamic social interactions in yeast. J. Evol. Biol. 21, 1836-1843 (2008).
74. Garcia-Vallve, S., Romeu, A. & Palau, J. Horizontal gene transfer of glycosyl hydrolases of the rumen fungi. Mol. Biol. Evol. 17, 352-361 (2000). (Pubitemid 30123756)
75. 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). (Pubitemid 38824032)
76. Richards, T. A., Leonard, G., Soanes, D. M. & Talbot, N. J. Gene transfer into the fungi. Fungal Biol. Rev. 25, 98-110 (2011).
77. 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). (Pubitemid 41070820)
78. Gabaldon, T. & Huynen, M. A. Reconstruction of the proto-mitochondrial metabolism. Science 301, 609 (2003). (Pubitemid 36927938)
79. Lawrence, J. G. Microbial evolution: enforcing cooperation by partial kin selection. Curr. Biol. 19, R943-R945 (2009).
80. 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). (Pubitemid 44354141)
81. 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).
82. Noll, K. M. & Thirangoon, K. Interdomain transfers of sugar transporters overcome barriers to gene expression. Methods Mol. Biol. 532, 309-322 (2009).
83. Hellborg, L., Woolfit, M., Arthursson-Hellborg, M. & Piskur, J. Complex evolution of the DAL5 transporter family. BMC Genomics 9, 164 (2008).
84. Gomolplitinant, K. M. & Saier, M. H. Jr. Evolution of the oligopeptide transporter family. J. Membr. Biol. 240, 89-110 (2011).
85. 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). (Pubitemid 34832576)
86. 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). (Pubitemid 47236698)
87. 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).
88. 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).
89. 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).
90. 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). (Pubitemid 29168991)
91. 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).
92. Uetz, P. et al. A comprehensive analysis of protein- protein interactions in Saccharomyces cerevisiae. Nature 403, 623-627 (2000). (Pubitemid 30103994)
93. Jeong, H., Mason, S. P., Barabasi, A. L. & Oltvai, Z. N. Lethality and centrality in protein networks. Nature 411, 41-42 (2001). (Pubitemid 32428180)
94. Stark, C. et al. BioGRID: a general repository for interaction datasets. Nucleic Acids Res. 34, D535-539 (2006).
95. 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).
96. 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).
97. 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).
98. Lehmann, L., Bargum, K. & Reuter, M. An evolutionary analysis of the relationship between spite and altruism. J. Evol. Biol. 19, 1507-1516 (2006).
99. Harrison, F. & Buckling, A. Siderophore production and biofilm formation as linked social traits. ISME J. 3, 632-634 (2009).
100. 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). (Pubitemid 47075145)
101. Fox, E. M. & Howlett, B. J. Secondary metabolism: regulation and role in fungal biology. Curr. Opin. Microbiol. 11, 481-487 (2008).
102. 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). (Pubitemid 28519891)
103. Friesen, T. L. et al. Emergence of a new disease as a result of interspecific virulence gene transfer. Nature Genet. 38, 953-956 (2006). (Pubitemid 44141666)
104. Patron, N. J. et al. Origin and distribution of epipolythiodioxopiperazine (ETP) gene clusters in filamentous ascomycetes. BMC Evol. Biol. 7, 174 (2007).
105. 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).
106. 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).