1932

Abstract

Here we review two connected themes in evolutionary microbiology: () the nature of gene repertoire variation within species groups (pangenomes) and () the concept of metabolite transporters as accessory proteins capable of providing niche-defining “bolt-on” phenotypes. We discuss the need for improved sampling and understanding of pangenome variation in eukaryotic microbes. We then review the factors that shape the repertoire of accessory genes within pangenomes. As part of this discussion, we outline how gene duplication is a key factor in both eukaryotic pangenome variation and transporter gene family evolution. We go on to outline how, through functional characterization of transporter-encoding genes, in combination with analyses of how transporter genes are gained and lost from accessory genomes, we can reveal much about the niche range, the ecology, and the evolution of virulence of microbes. We advocate for the coordinated systematic study of eukaryotic pangenomes through genome sequencing and the functional analysis of genes found within the accessory gene repertoire.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-032421-115538
2023-09-15
2024-12-04
Loading full text...

Full text loading...

/deliver/fulltext/micro/77/1/annurev-micro-032421-115538.html?itemId=/content/journals/10.1146/annurev-micro-032421-115538&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Andreani NA, Hesse E, Vos M. 2017. Prokaryote genome fluidity is dependent on effective population size. ISME J 11:71719–21
    [Google Scholar]
  2. 2.
    Badet T, Croll D. 2020. The rise and fall of genes: origins and functions of plant pathogen pangenomes. Curr. Opin. Plant Biol. 56:65–73
    [Google Scholar]
  3. 3.
    Badet T, Oggenfuss U, Abraham L, McDonald BA, Croll D. 2020. A 19-isolate reference-quality global pangenome for the fungal wheat pathogen Zymoseptoria tritici. BMC Biol 18:112
    [Google Scholar]
  4. 4.
    Baxter L, Tripathy S, Ishaque N, Boot N, Cabral A et al. 2010. Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science 330:60101549–51
    [Google Scholar]
  5. 5.
    Blanc-Mathieu R, Krasovec M, Hebrard M, Yau S, Desgranges E et al. 2017. Population genomics of picophytoplankton unveils novel chromosome hypervariability. Sci. Adv. 3:7e1700239
    [Google Scholar]
  6. 6.
    Boles E, Hollenberg CP. 1997. The molecular genetics of hexose transport in yeasts. FEMS Microbiol. Rev. 21:185–111
    [Google Scholar]
  7. 7.
    Brockhurst MA, Harrison E, Hall JPJ, Richards T, McNally A, MacLean C. 2019. The ecology and evolution of pangenomes. Curr. Biol. 29:20R1094–103
    [Google Scholar]
  8. 8.
    Brown CJ, Todd KM, Rosenzweig RF 1998. Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment. Mol. Biol. Evol. 15:8931–42Foundational work showing expansion in hexose transporters underpins adaptation to low sugar environments in yeast. Should be taught alongside peppered moths and Darwin's finches.
    [Google Scholar]
  9. 9.
    Cohen O, Gophna U, Pupko T 2011. The complexity hypothesis revisited: Connectivity rather than function constitutes a barrier to horizontal gene transfer. Mol. Biol. Evol. 28:41481–89HGT, and therefore accessory genome composition, is shaped by how the protein encoded by the transferred gene interacts with the wider proteome network.
    [Google Scholar]
  10. 10.
    Cordero OX, Ventouras L-A, DeLong EF, Polz MF. 2012. Public good dynamics drive evolution of iron acquisition strategies in natural bacterioplankton populations. PNAS 109:4920059–64
    [Google Scholar]
  11. 11.
    Cotton JA, McInerney JO. 2010. Eukaryotic genes of archaebacterial origin are more important than the more numerous eubacterial genes, irrespective of function. PNAS 107:4017252–55
    [Google Scholar]
  12. 12.
    Croft MT, Warren MJ, Smith AG. 2006. Algae need their vitamins. Eukaryot. Cell. 5:81175–83
    [Google Scholar]
  13. 13.
    Croll D, McDonald BA. 2012. The accessory genome as a cradle for adaptive evolution in pathogens. PLOS Pathog 8:4e1002608
    [Google Scholar]
  14. 14.
    Danhof HA, Lorenz MC. 2015. The Candida albicans ATO gene family promotes neutralization of the macrophage phagolysosome. Infect. Immun. 83:114416–26
    [Google Scholar]
  15. 15.
    Dean P, Sendra KM, Williams TA, Watson AK, Major P et al. 2018. Transporter gene acquisition and innovation in the evolution of Microsporidia intracellular parasites. Nat. Commun. 9:11709
    [Google Scholar]
  16. 16.
    Ding W, Baumdicker F, Neher RA. 2018. panX: pan-genome analysis and exploration. Nucleic Acids Res 46:1e5
    [Google Scholar]
  17. 17.
    Doolittle WF. 2008. Microbial evolution: stalking the wild bacterial species. Curr. Biol. 18:13R565–67
    [Google Scholar]
  18. 18.
    El-Sayed NM, Myler PJ, Blandin G, Berriman M, Crabtree J et al. 2005. Comparative genomics of trypanosomatid parasitic protozoa. Science 309:5733404–9
    [Google Scholar]
  19. 19.
    Etten JV, Bhattacharya D. 2020. Horizontal gene transfer in eukaryotes: not if, but how much?. Trends Genet 36:12915–25
    [Google Scholar]
  20. 20.
    Eyres I, Boschetti C, Crisp A, Smith TP, Fontaneto D et al. 2015. Horizontal gene transfer in bdelloid rotifers is ancient, ongoing and more frequent in species from desiccating habitats. BMC Biol 13:90
    [Google Scholar]
  21. 21.
    Fan X, Qiu H, Han W, Wang Y, Xu D et al. 2020. Phytoplankton pangenome reveals extensive prokaryotic horizontal gene transfer of diverse functions. Sci. Adv. 6:18eaba0111
    [Google Scholar]
  22. 22.
    Fickers P, Benetti P-H, Waché Y, Marty A, Mauersberger S et al. 2005. Hydrophobic substrate utilisation by the yeast Yarrowia lipolytica, and its potential applications. FEMS Yeast Res 5:6–7527–43
    [Google Scholar]
  23. 23.
    Fisher SK, Novak JE, Agranoff BW. 2002. Inositol and higher inositol phosphates in neural tissues: homeostasis, metabolism and functional significance. J. Neurochem. 82:4736–54
    [Google Scholar]
  24. 24.
    Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H et al. 2006. Emergence of a new disease as a result of interspecific virulence gene transfer. Nat. Genet 38:8953–56Evidence of recent HGT between plant-associated fungi that expands the accessory genome and drives pathogenicity.
    [Google Scholar]
  25. 25.
    González-Pech RA, Stephens TG, Chen Y, Mohamed AR, Cheng Y et al. 2021. Comparison of 15 dinoflagellate genomes reveals extensive sequence and structural divergence in family Symbiodiniaceae and genus Symbiodinium. BMC Biol 19:173
    [Google Scholar]
  26. 26.
    Greiner T, Moroni A, Van Etten JL, Thiel G. 2018. Genes for membrane transport proteins: not so rare in viruses. Viruses 10:9456
    [Google Scholar]
  27. 27.
    Hatta R, Ito K, Hosaki Y, Tanaka T, Tanaka A et al. 2002. A conditionally dispensable chromosome controls host-specific pathogenicity in the fungal plant pathogen Alternaria alternata. Genetics 161:159–70
    [Google Scholar]
  28. 28.
    He C, Rusu AG, Poplawski AM, Irwin JAG, Manners JM. 1998. Transfer of a supernumerary chromosome between vegetatively incompatible biotypes of the fungus Colletotrichum gloeosporioides. Genetics 150:41459–66
    [Google Scholar]
  29. 29.
    Heinz E, Hacker C, Dean P, Mifsud J, Goldberg AV et al. 2014. Plasma membrane-located purine nucleotide transport proteins are key components for host exploitation by microsporidian intracellular parasites. PLOS Pathog 10:12e1004547
    [Google Scholar]
  30. 30.
    Hu J, Chen C, Peever T, Dang H, Lawrence C, Mitchell T 2012. Genomic characterization of the conditionally dispensable chromosome in Alternaria arborescens provides evidence for horizontal gene transfer. BMC Genom 13:1171
    [Google Scholar]
  31. 31.
    Hughes T, Ekman D, Ardawatia H, Elofsson A, Liberles DA. 2007. Evaluating dosage compensation as a cause of duplicate gene retention in Paramecium tetraurelia. Genome Biol 8:5213
    [Google Scholar]
  32. 32.
    Husnik F, McCutcheon JP. 2018. Functional horizontal gene transfer from bacteria to eukaryotes. Nat. Rev. Microbiol. 16:267–79
    [Google Scholar]
  33. 33.
    Inderbitzin P, Harkness J, Turgeon BG, Berbee ML. 2005. Lateral transfer of mating system in Stemphylium. PNAS 102:3211390–95
    [Google Scholar]
  34. 34.
    Innan H, Kondrashov F. 2010. The evolution of gene duplications: classifying and distinguishing between models. Nat. Rev. Genet. 11:297–108
    [Google Scholar]
  35. 35.
    Irwin NAT, Pittis AA, Richards TA, Keeling PJ. 2022. Systematic evaluation of horizontal gene transfer between eukaryotes and viruses. Nat. Microbiol. 7:2327–36
    [Google Scholar]
  36. 36.
    Jain R, Rivera MC, Lake JA. 1999. Horizontal gene transfer among genomes: the complexity hypothesis. PNAS 96:73801–6
    [Google Scholar]
  37. 37.
    Jeong H, Mason SP, Barabási A-L, Oltvai ZN. 2001. Lethality and centrality in protein networks. Nature 411:683341–42
    [Google Scholar]
  38. 38.
    Jordan P, Choe J-Y, Boles E, Oreb M. 2016. Hxt13, Hxt15, Hxt16 and Hxt17 from Saccharomyces cerevisiae represent a novel type of polyol transporters. Sci. Rep. 6:123502
    [Google Scholar]
  39. 39.
    Katinka MD, Duprat S, Cornillot E, Méténier G, Thomarat F et al. 2001. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414:6862450–53
    [Google Scholar]
  40. 40.
    Keeling PJ, Inagaki Y. 2004. A class of eukaryotic GTPase with a punctate distribution suggesting multiple functional replacements of translation elongation factor 1α. PNAS 101:4315380–85
    [Google Scholar]
  41. 41.
    Kondrashov FA. 2012. Gene duplication as a mechanism of genomic adaptation to a changing environment. Proc. Biol. Sci. 279: 1749.5048–57
    [Google Scholar]
  42. 42.
    Krogh A, Larsson B, von Heijne G, Sonnhammer ELL. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305:3567–80
    [Google Scholar]
  43. 43.
    Lercher MJ, Pal C. 2008. Integration of horizontally transferred genes into regulatory interaction networks takes many million years. Mol. Biol. Evol. 25:3559–67
    [Google Scholar]
  44. 44.
    Lessard EJ, Merico A, Tyrrell T. 2005. Nitrate: phosphate ratios and Emiliania huxleyi blooms. Limnol. Oceanogr. 50:31020–24
    [Google Scholar]
  45. 45.
    Li G, Ji B, Nielsen J 2019. The pan-genome of Saccharomyces cerevisiae. FEMS Yeast Res 19:7foz064
    [Google Scholar]
  46. 46.
    Li H, Li Y, Sun T, Du W, Li C et al. 2019. Unveil the transcriptional landscape at the Cryptococcus-host axis in mice and nonhuman primates. PLOS Negl. Trop. Dis. 13:7e0007566
    [Google Scholar]
  47. 47.
    Lindsay RJ, Pawlowska BJ, Gudelj I. 2019. Privatization of public goods can cause population decline. Nat. Ecol. Evol. 3:81206–16
    [Google Scholar]
  48. 48.
    Liu G, Yong MYJ, Yurieva M, Srinivasan KG, Liu J et al. 2015. Gene essentiality is a quantitative property linked to cellular evolvability. Cell 163:61388–99
    [Google Scholar]
  49. 49.
    Liu T-B, Kim J-C, Wang Y, Toffaletti DL, Eugenin E et al. 2013. Brain inositol is a novel stimulator for promoting Cryptococcus penetration of the blood-brain barrier. PLOS Pathog 9:4e1003247
    [Google Scholar]
  50. 50.
    Logeman BL, Wood LK, Lee J, Thiele DJ. 2017. Gene duplication and neo-functionalization in the evolutionary and functional divergence of the metazoan copper transporters Ctr1 and Ctr2. J. Biol. Chem. 292:2711531–46
    [Google Scholar]
  51. 51.
    Ma L-J, van der Does HC, Borkovich KA, Coleman JJ, Daboussi M-J et al. 2010. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464:7287367–73Key demonstration that fungi can place major units of their accessory genomes in accessory chromosomes, and that these are mobile between evolutionary lineages.
    [Google Scholar]
  52. 52.
    MacLean RC, Gudelj I. 2006. Resource competition and social conflict in experimental populations of yeast. Nature 441:7092498–501
    [Google Scholar]
  53. 53.
    Major P, Sendra KM, Dean P, Williams TA, Watson AK et al. 2019. A new family of cell surface located purine transporters in Microsporidia and related fungal endoparasites. eLife 8:e47037
    [Google Scholar]
  54. 54.
    Marini AM, Soussi-Boudekou S, Vissers S, Andre B. 1997. A family of ammonium transporters in Saccharomyces cerevisiae. Mol. Cell. Biol. 17:84282–93
    [Google Scholar]
  55. 55.
    Martho KFC, de Melo AT, Takahashi JPF, Guerra JM, da Silva, Santos DC et al. 2016. Amino acid permeases and virulence in Cryptococcus neoformans. PLOS ONE 11:10e0163919
    [Google Scholar]
  56. 56.
    McCarthy CGP, Fitzpatrick DA. 2019. Pan-genome analyses of model fungal species. Microb. Genom. 5:2e000243Systematic comparisons of eukaryotic pangenomes reveal that gene duplications are an important factor.
    [Google Scholar]
  57. 57.
    McCarthy CGP, Fitzpatrick DA. 2019. Pangloss: a tool for pan-genome analysis of microbial eukaryotes. Genes 10:7521
    [Google Scholar]
  58. 58.
    McInerney JO, McNally A, O'Connell MJ 2017. Why prokaryotes have pangenomes. Nat. Microbiol. 2:17040
    [Google Scholar]
  59. 59.
    McKie-Krisberg ZM, Sanders RW. 2014. Phagotrophy by the picoeukaryotic green alga Micromonas: implications for Arctic Oceans. ISME J 8:101953–61
    [Google Scholar]
  60. 60.
    Milner DS, Attah V, Cook E, Maguire F, Savory FR et al. 2019. Environment-dependent fitness gains can be driven by horizontal gene transfer of transporter-encoding genes. PNAS 116:125613–22
    [Google Scholar]
  61. 61.
    Milner DS, Wideman JG, Stairs CW, Dunn CD, Richards TA. 2021. A functional bacteria-derived restriction modification system in the mitochondrion of a heterotrophic protist. PLOS Biol 19:4e3001126
    [Google Scholar]
  62. 62.
    Monier A, Chambouvet A, Milner DS, Attah V, Terrado R et al. 2017. Host-derived viral transporter protein for nitrogen uptake in infected marine phytoplankton. PNAS 114:36E7489–98
    [Google Scholar]
  63. 63.
    Monier A, Welsh RM, Gentemann C, Weinstock G, Sodergren E et al. 2012. Phosphate transporters in marine phytoplankton and their viruses: cross-domain commonalities in viral-host gene exchanges. Environ. Microbiol. 14:1162–76Virus genomes carry variant transporter genes, providing a key hint that viruses are acting to drive gene transfer and therefore act to further provision eukaryotic accessory genomes.
    [Google Scholar]
  64. 64.
    Morris JJ, Lenski RE, Zinser ER. 2012. The Black Queen Hypothesis: evolution of dependencies through adaptive gene loss. mBio 3:2e00036–12
    [Google Scholar]
  65. 65.
    Navarathna DHMLP, Das A, Morschhäuser J, Nickerson KW, Roberts DD. 2011. Dur3 is the major urea transporter in Candida albicans and is co-regulated with the urea amidolyase Dur1,2. Microbiology 157:Part 1270–79
    [Google Scholar]
  66. 66.
    Ngamskulrungroj P, Chang Y, Sionov E, Kwon-Chung KJ. 2012. The primary target organ of Cryptococcus gattii is different from that of Cryptococcus neoformans in a murine model. mBio 3:3e00103–12
    [Google Scholar]
  67. 67.
    Norsigian CJ, Danhof HA, Brand CK, Midani FS, Broddrick JT et al. 2022. Systems biology approach to functionally assess the Clostridioides difficile pangenome reveals genetic diversity with discriminatory power. PNAS 119:18e2119396119
    [Google Scholar]
  68. 68.
    Ohno S. 1970. Evolution by Gene Duplication Berlin: Springer
    [Google Scholar]
  69. 69.
    Oliveira PH, Touchon M, Rocha EPC. 2016. Regulation of genetic flux between bacteria by restriction-modification systems. PNAS 113:205658–63
    [Google Scholar]
  70. 70.
    Osuna-Cruz CM, Bilcke G, Vancaester E, De Decker S, Bones AM et al. 2020. The Seminavis robusta genome provides insights into the evolutionary adaptations of benthic diatoms. Nat. Commun. 11:13320
    [Google Scholar]
  71. 71.
    Otterstedt K, Larsson C, Bill RM, Ståhlberg A, Boles E et al. 2004. Switching the mode of metabolism in the yeast Saccharomyces cerevisiae. EMBO Rep 5:5532–37
    [Google Scholar]
  72. 72.
    Oughtred R, Rust J, Chang C, Breitkreutz B-J, Stark C et al. 2021. The BioGRID database: A comprehensive biomedical resource of curated protein, genetic, and chemical interactions. Protein Sci 30:1187–200
    [Google Scholar]
  73. 73.
    Papp B, Pál C, Hurst LD. 2003. Dosage sensitivity and the evolution of gene families in yeast. Nature 424:6945194–97
    [Google Scholar]
  74. 74.
    Peck KM, Lauring AS. 2018. Complexities of viral mutation rates. Virol. J. 92:14e01031–17
    [Google Scholar]
  75. 75.
    Plissonneau C, Hartmann FE, Croll D. 2018. Pangenome analyses of the wheat pathogen Zymoseptoria tritici reveal the structural basis of a highly plastic eukaryotic genome. BMC Biol 16:5
    [Google Scholar]
  76. 76.
    Poulsen BE, Yang R, Clatworthy AE, White T, Osmulski SJ et al. 2019. Defining the core essential genome of Pseudomonas aeruginosa. PNAS 116:2010072–80
    [Google Scholar]
  77. 77.
    Rajasingham R, Smith RM, Park BJ, Jarvis JN, Govender NP et al. 2017. Global burden of disease of HIV-associated cryptococcal meningitis: an updated analysis. Lancet Infect Dis 17:8873–81
    [Google Scholar]
  78. 78.
    Rastogi A, Vieira FRJ, Deton-Cabanillas A-F, Veluchamy A, Cantrel C et al. 2020. A genomics approach reveals the global genetic polymorphism, structure, and functional diversity of ten accessions of the marine model diatom Phaeodactylum tricornutum. ISME J 14:2347–63
    [Google Scholar]
  79. 79.
    Read BA, Kegel J, Klute MJ, Kuo A, Lefebvre SC et al. 2013. Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature 499:7457209–13
    [Google Scholar]
  80. 80.
    Rees DC, Johnson E, Lewinson O 2009. ABC transporters: the power to change. Nat. Rev. Mol. Cell. Biol. 10:3218–27
    [Google Scholar]
  81. 81.
    Reis AC, Cunha MV. 2021. The open pan-genome architecture and virulence landscape of Mycobacterium bovis. Microb. Genom. 7:10000664
    [Google Scholar]
  82. 82.
    Reno ML, Held NL, Fields CJ, Burke PV, Whitaker RJ. 2009. Biogeography of the Sulfolobus islandicus pan-genome. PNAS 106:218605–10
    [Google Scholar]
  83. 83.
    Richards TA, Leonard G, Soanes DM, Talbot NJ. 2011. Gene transfer into the fungi. Fungal Biol. Rev. 25:298–110
    [Google Scholar]
  84. 84.
    Richards TA, Talbot NJ. 2013. Horizontal gene transfer in osmotrophs: playing with public goods. Nat. Rev. Microbiol. 11:10720–27
    [Google Scholar]
  85. 85.
    Richards TA, Talbot NJ. 2018. Osmotrophy. Curr. Biol. 28:20R1179–80
    [Google Scholar]
  86. 86.
    Rokitta SD, Von Dassow P, Rost B, John U 2014. Emiliania huxleyi endures N-limitation with an efficient metabolic budgeting and effective ATP synthesis. BMC Genom 15:11051
    [Google Scholar]
  87. 87.
    Rolland F, Winderickx J, Thevelein JM. 2002. Glucose-sensing and -signalling mechanisms in yeast. FEMS Yeast Res 2:2183–201
    [Google Scholar]
  88. 88.
    Rousset F, Cabezas-Caballero J, Piastra-Facon F, Fernández-Rodríguez J, Clermont O et al. 2021. The impact of genetic diversity on gene essentiality within the Escherichia coli species. Nat. Microbiol. 6:3301–12
    [Google Scholar]
  89. 89.
    Roux S, Brum JR, Dutilh BE, Sunagawa S, Duhaime MB et al. 2016. Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature 537:7622689–93
    [Google Scholar]
  90. 90.
    Ryan CJ, Krogan NJ, Cunningham P, Cagney G. 2013. All or nothing: protein complexes flip essentiality between distantly related eukaryotes. Genome Biol. Evol. 5:61049–59
    [Google Scholar]
  91. 91.
    Saier MH, Reddy VS, Moreno-Hagelsieb G, Hendargo KJ, Zhang Y et al. 2021. The transporter classification database (TCDB): 2021 update. Nucleic Acids Res 49:D1D461–67
    [Google Scholar]
  92. 92.
    Savory FR, Milner DS, Miles DC, Richards TA. 2018. Ancestral function and diversification of a horizontally acquired oomycete carboxylic acid transporter. Mol. Biol. Evol. 35:81887–900
    [Google Scholar]
  93. 93.
    Seabolt MH, Roellig DM, Konstantinidis KT. 2022. Genomic comparisons confirm Giardia duodenalis sub-assemblage AII as a unique species. Front. Cell. Infect. Microbiol. 12:1010244
    [Google Scholar]
  94. 94.
    Shapiro BJ 2017. The population genetics of pangenomes. Nat. Microbiol. 2:121574Constructive discussion about whether accessory genomes are neutral or adaptive.
    [Google Scholar]
  95. 95.
    Sharma S, Markham PF, Browning GF. 2014. Genes found essential in other mycoplasmas are dispensable in Mycoplasma bovis. PLOS ONE 9:6e97100
    [Google Scholar]
  96. 96.
    Slot JC, Gluck-Thaler E. 2019. Metabolic gene clusters, fungal diversity, and the generation of accessory functions. Curr. Opin. Genet. Dev. 58–59:17–24
    [Google Scholar]
  97. 97.
    Szabová J, Ruzicka P, Verner Z, Hampl V, Lukes J. 2011. Experimental examination of EFL and MATX eukaryotic horizontal gene transfers: coexistence of mutually exclusive transcripts predates functional rescue. Mol. Biol. Evol. 28:82371–78
    [Google Scholar]
  98. 98.
    Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D et al. 2005. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome. .” PNAS 102:3913950–55
    [Google Scholar]
  99. 99.
    Tonkin-Hill G, MacAlasdair N, Ruis C, Weimann A, Horesh G et al. 2020. Producing polished prokaryotic pangenomes with the Panaroo pipeline. Genome Biol 21:1180
    [Google Scholar]
  100. 100.
    Vakirlis N, Hebert AS, Opulente DA, Achaz G, Hittinger CT et al. 2018. A molecular portrait of de novo genes in yeasts. Mol. Biol. Evol. 35:3631–45
    [Google Scholar]
  101. 101.
    Verduyn C, Zomerdijk TPL, van Dijken JP, Scheffers WA. 1984. Continuous measurement of ethanol production by aerobic yeast suspensions with an enzyme electrode. Appl. Microbiol. Biotechnol. 19:3181–85
    [Google Scholar]
  102. 102.
    Vylkova S, Carman AJ, Danhof HA, Collette JR, Zhou H, Lorenz MC. 2011. The fungal pathogen Candida albicans autoinduces hyphal morphogenesis by raising extracellular pH. mBio 2:3e00055–11
    [Google Scholar]
  103. 103.
    Weir W, Capewell P, Foth B, Clucas C, Pountain A et al. 2016. Population genomics reveals the origin and asexual evolution of human infective trypanosomes. eLife 5:e11473
    [Google Scholar]
  104. 104.
    Whelan FJ, Hall RJ, McInerney JO. 2021. Evidence for selection in the abundant accessory gene content of a prokaryote pangenome. Mol. Biol. Evol. 38:93697–708
    [Google Scholar]
  105. 105.
    Whittaker RH. 1969. New concepts of kingdoms or organisms: Evolutionary relations are better represented by new classifications than by the traditional two kingdoms. Science 163:3863150–60
    [Google Scholar]
  106. 106.
    Williams TA, Nakjang S, Campbell SE, Freeman MA, Eydal M et al. 2016. A recent whole-genome duplication divides populations of a globally distributed microsporidian. Mol. Biol. Evol. 33:82002–15
    [Google Scholar]
  107. 107.
    Worden AZ, Lee J-H, Mock T, Rouzé P, Simmons MP et al. 2009. Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324:5924268–72
    [Google Scholar]
  108. 108.
    Xue C, Liu T, Chen L, Li W, Liu I et al. 2010. Role of an expanded inositol transporter repertoire in Cryptococcus neoformans sexual reproduction and virulence. mBio 1:1e00084–10Important example of how transporter evolution can shape the evolution of a parasitic fungus.
    [Google Scholar]
  109. 109.
    Zhang Z, Ren Q. 2020. Why are essential genes essential? The essentiality of Saccharomyces genes. Microb. Cell 2:8280–87
    [Google Scholar]
  110. 110.
    Zhu Y, Du P, Nakhleh L. 2012. Gene duplicability-connectivity-complexity across organisms and a neutral evolutionary explanation. PLOS ONE 7:9e44491
    [Google Scholar]
/content/journals/10.1146/annurev-micro-032421-115538
Loading
/content/journals/10.1146/annurev-micro-032421-115538
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error