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Phylogenetic conservatism of thermal traits explains dispersal limitation and genomic differentiation of Streptomyces sister-taxa

The ISME Journalvolume 12pages21762186 (2018) | Download Citation

Abstract

The latitudinal diversity gradient is a pattern of biogeography observed broadly in plants and animals but largely undocumented in terrestrial microbial systems. Although patterns of microbial biogeography across broad taxonomic scales have been described in a range of contexts, the mechanisms that generate biogeographic patterns between closely related taxa remain incompletely characterized. Adaptive processes are a major driver of microbial biogeography, but there is less understanding of how microbial biogeography and diversification are shaped by dispersal limitation and drift. We recently described a latitudinal diversity gradient of species richness and intraspecific genetic diversity in Streptomyces by using a geographically explicit culture collection. Within this geographically explicit culture collection, we have identified Streptomyces sister-taxa whose geographic distribution is delimited by latitude. These sister-taxa differ in geographic distribution, genomic diversity, and ecological traits despite having nearly identical SSU rRNA gene sequences. Comparative genomic analysis reveals genomic differentiation of these sister-taxa consistent with restricted gene flow across latitude. Furthermore, we show phylogenetic conservatism of thermal traits between the sister-taxa suggesting that thermal trait adaptation limits dispersal and gene flow across climate regimes as defined by latitude. Such phylogenetic conservatism of thermal traits is commonly associated with latitudinal diversity gradients for plants and animals. These data provide further support for the hypothesis that the Streptomyces latitudinal diversity gradient was formed as a result of historical demographic processes defined by dispersal limitation and driven by paleoclimate dynamics.

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References

  1. 1.

    Hillebrand H. On the generality of the latitudinal diversity gradient. Am Nat. 2004;163:192–211.

  2. 2.

    Fuhrman JA, Steele JA, Hewson I, Schwalbach MS, Brown MV, Green JL, et al. A latitudinal diversity gradient in planktonic marine bacteria. Proc Natl Acad Sci USA. 2008;105:7774–8.

  3. 3.

    Pommier T, Canbäck B, Riemann L, Boström KH, Simu K, Lundberg P, et al. Global patterns of diversity and community structure in marine bacterioplankton. Mol Ecol. 2006;16:867–80.

  4. 4.

    Sul WJ, Oliver TA, Ducklow HW, Amaral-Zettler LA, Sogin ML. Marine bacteria exhibit a bipolar distribution. Proc Natl Acad Sci USA. 2013;110:2342–7.

  5. 5.

    Swan BK, Tupper B, Sczyrba A, Lauro FM, Martinez-Garcia M, Gonzalez JM, et al. Prevalent genome streamlining and latitudinal divergence of planktonic bacteria in the surface ocean. Proc Natl Acad Sci USA. 2013;110:11463–8.

  6. 6.

    Andam CP, Choudoir MJ, Nguyen VA, Park SH, Buckley DH. Contributions of ancestral inter-species recombination to the genetic diversity of extant Streptomyces lineages. ISME J. 2016a;10:1731–41.

  7. 7.

    Andam CP, Doroghazi JR, Campbell AN, Kelly PJ, Choudoir MJ, Buckley DH. A latitudinal diversity gradient in terrestrial bacteria of the genus Streptomyces. mBio. 2016b;7:e02200–15.

  8. 8.

    Zhou J, Deng Y, Shen L, Wen C, Yan Q, Ning D, et al. Temperature mediates continental-scale diversity of microbes in forest soils. Nat Commun. 2016;7:12083.

  9. 9.

    Fierer N, Lennon JT. The generation and maintenance of diversity in microbial communities. Am J Bot. 2011;98:439–48.

  10. 10.

    Green J, Bohannan BJM. Spatial scaling of microbial biodiversity. Trends Ecol Evol. 2006;21:501–7.

  11. 11.

    Locey KJ, Lennon JT. Scaling laws predict global microbial diversity. Proc Natl Acad Sci USA. 2016;113:5970–5.

  12. 12.

    Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, et al. Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol. 2006;4:102–12.

  13. 13.

    Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JBH. Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol. 2012;10:247–506.

  14. 14.

    Choudoir MJ, Campbell AN, Buckley DH. Grappling with Proteus: population level approaches to understanding microbial diversity. Front Microbiol. 2012;3:336.

  15. 15.

    Finlay BJ. Global dispersal of free-living microbial Eukaryote species. Science. 2002;296:1061–3.

  16. 16.

    Finlay BJ, Fenchel T. Cosmopolitan metapopulations of free-living microbial eukaryotes. Protist. 2004;155:237–44.

  17. 17.

    Mittelbach GG, Schemske DW, Cornell HV, Allen AP, Brown JM, Bush MB, et al. Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecol Lett. 2007;10:315–31.

  18. 18.

    Pianka EricR. Latitudinal gradients in species diversity: a review of concepts. Am Nat. 1966;100:33–46.

  19. 19.

    Currie DJ, Mittelbach GG, Cornell HV, Field R, Guegan J-F, Hawkins BA, et al. Predictions and tests of climate-based hypotheses of broad-scale variation in taxonomic richness. Ecol Lett. 2004;7:1121–34.

  20. 20.

    Field R, Hawkins BA, Cornell HV, Currie DJ, Diniz-Filho JAF, Guégan J-F, et al. Spatial species-richness gradients across scales: a meta-analysis. J Biogeogr. 2009;36:132–47.

  21. 21.

    Allen AP, Brown JH, Gillody JF. Global biodiversity, biochemical kinetics, and the energetic-equivalence rule. Science. 2002;297:1545–8.

  22. 22.

    Stevens RD. Historical processes enhance patterns of diversity along latitudinal gradients. Proc Biol Sci. 2006;273:2283–9.

  23. 23.

    Wiens JJ, Donoghue MJ. Historical biogeography, ecology and species richness. Trends Ecol Evol. 2004;19:639–44.

  24. 24.

    Stephens PR, Wiens JJ. Explaining species richness from continents to communities: the time‐for‐speciation effect in Emydid turtles. Am Nat. 2003;161:112–28.

  25. 25.

    Hewitt GM. Some genetic consequences of ice ages, and their role, in divergence and speciation. Biol J Linn Soc Lond. 1996;58:247–76.

  26. 26.

    Choudoir MJ, Doroghazi JR, Buckley DH. Latitude delineates patterns of biogeography in terrestrial Streptomyces. Environ Microbiol. 2016;18:4931–45.

  27. 27.

    Kenefic LJ, Pearson T, Okinaka RT, Schupp JM, Wagner DM, Ravel J, et al. Pre-Columbian origins for North American anthrax. PLoS ONE. 2009;4:e4813.

  28. 28.

    Eisenlord SD, Zak DR, Upchurch RA. Dispersal limitation and the assembly of soil Actinobacteria communities in a long-term chronosequence. Ecol Evol. 2012;2:538–49.

  29. 29.

    Delgado-Baquerizo M, Bissett A, Eldridge DJ, Maestre FT, He J-Z, Wang J-T, et al. Palaeoclimate explains a unique proportion of the global variation in soil bacterial communities. Nat Ecol Evol. 2017;1:1339–47.

  30. 30.

    Kämpfer P. The family Streptomycetaceae Part I: taxonomy. The Prokaryotes. New York, NY: Springer; 2006. p. 538–604. Vol. 3

  31. 31.

    Kieser T, Bibb MJ, Buttner MJ, Charter KF, Hopwood DA. Practical Streptomyces Genetics. Norwich, UK: John Innes Foundation; 2000.

  32. 32.

    Ljungdhal LG, Eriksson K. The ecology of microbial cellulose degradation. In: Advances in microbial ecology. Vol. 8. Springer:New York, USA; 1985. p. 237–99.

  33. 33.

    Schrempf H. Recognition and degradation of chitin by streptomycetes. Antonie Van Leeuwenhoek. 2001;79:285–9.

  34. 34.

    Watve M, Tickoo R, Jog M, Bhole B. How many antibiotics are produced by the genus Streptomyces? Arch Microbiol. 2001;176:386–90.

  35. 35.

    Waters JM, Fraser CI, Hewitt GM. Founder takes all: density-dependent processes structure biodiversity. Trends Ecol Evol. 2013;28:78–85.

  36. 36.

    Crisp MD, Cook LG. Phylogenetic niche conservatism: what are the underlying evolutionary and ecological causes? New Phytol. 2012;196:681–94.

  37. 37.

    Wiens JJ, Ackerly DD, Allen AP, Anacker BL, Buckley LB, Cornell HV, et al. Niche conservatism as an emerging principle in ecology and conservation biology. Ecol Lett. 2010;13:1310–24.

  38. 38.

    El-Nakeeb MA, Lechevalier HA. Selective isolation of aerobic Actinomycetes. Appl Microbiol. 1963;11:75–55.

  39. 39.

    Ottow JCG. Rose bengal as a selective aid in the isolation of fungi and Actinomycetes from natural sources. Mycologia. 1972;64:304.

  40. 40.

    Doroghazi JR, Buckley DH. Widespread homologous recombination within and between Streptomyces species. ISME J. 2010;4:1136–43.

  41. 41.

    Roberts MA, Crawford DL. Use of randomly amplified polymorphic DNA as a means of developing genus-and strain-specific Streptomyces DNA probes. Appl Environ Microbiol. 2000;66:2555–64.

  42. 42.

    Tritt A, Eisen JA, Facciotti MT, Darling AE. An integrated pipeline for de novo assembly of microbial genomes. PLoS ONE. 2012;7:e42304.

  43. 43.

    Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, et al. The RAST server: rapid annotations using subsystems technology. BMC Genom. 2008;9:75.

  44. 44.

    Benedict MN, Henriksen JR, Metcalf WW, Whitaker RJ, Price ND. ITEP: an integrated toolkit for exploration of microbial pan-genomes. BMC Genom. 2014;15:8.

  45. 45.

    Angiuoli SV, Salzberg SL. Mugsy: fast multiple alignment of closely related whole genomes. Bioinformatics. 2011;27:334–42.

  46. 46.

    Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25:1972–3.

  47. 47.

    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75:7537–41.

  48. 48.

    Tavaré S. Some probabilistic and statistical problems in the analysis of DNA sequences. Lectures on Mathematics in the Life Sciences, American Mathematical Society. 1986;17:57–86.

  49. 49.

    Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22:2688–90.

  50. 50.

    Stamatakis A, Hoover P, Rougemont J, Renner S. A rapid bootstrap algorithm for the RAxML web servers. Syst Biol. 2008;57:758–71.

  51. 51.

    Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–80.

  52. 52.

    Excoffier L, Lischer HEL. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 2010;10:564–7.

  53. 53.

    Paradis E. pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics. 2010;26:419–20.

  54. 54.

    Paradis E, Claude J, Strimmer K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics. 2004;20:289–90.

  55. 55.

    Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 2007;56:564–77.

  56. 56.

    Kämpfer P, Kroppenstedt RM, Dott W. A numerical classification of the genera Streptomyces and Streptoverticillium using miniaturized physiological tests. Microbiology. 1991;137:1831–91.

  57. 57.

    Sambrook J, Russell RW. Molecular cloning: a laboratory manual. 3rd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 2001.

  58. 58.

    Konstantinidis KT, Tiedje JM. Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci USA. 2005;102:2567–72.

  59. 59.

    Hewitt GM. Genetic consequences of climatic oscillations in the Quaternary. Philos Trans R Soc Lond B Biol Sci. 2004;359:183–95.

  60. 60.

    Shafer ABA, Cullingham CI, Côté SD, Coltman DW. Of glaciers and refugia: a decade of study sheds new light on the phylogeography of northwestern North America. Mol Ecol. 2010;19:4589–621.

  61. 61.

    Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM. DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol. 2007;57:81–91.

  62. 62.

    Hawkins BA, Porter EE. Relative influences of current and historical factors on mammal and bird diversity patterns in deglaciated North America. Glob Ecol Biogeogr. 2003;12:475–81.

  63. 63.

    Adams RI, Hadly EA. Genetic diversity within vertebrate species is greater at lower latitudes. Evol Ecol. 2013;27:133–43.

  64. 64.

    Bernatchez L, Wilson CC. Comparative phylogeography of Nearctic and Palearctic fishes. Mol Ecol. 1998;7:431–52.

  65. 65.

    Gogarten JP, Doolittle WF, Lawrence JG. Prokaryotic evolution in light of gene transfer. Mol Biol Evol. 2002;19:2226–38.

  66. 66.

    Ochman H, Lawrence JG, Groisman EA. Lateral gene transfer and the nature of bacterial innovation. Nature. 2000;405:299.

  67. 67.

    Doroghazi JR, Buckley DH. Intraspecies comparison of Streptomyces pratensis genomes reveals high levels of recombination and gene conservation between strains of disparate geographic origin. BMC Genom. 2014;15:970.

  68. 68.

    Fraser C, Hanage WP, Spratt BG. Recombination and the nature of bacterial speciation. Science. 2007;315:476–80.

  69. 69.

    Krause DJ, Whitaker RJ. Inferring speciation processes from patterns of natural variation in microbial genomes. Syst Biol. 2015;64:926–35.

  70. 70.

    Shapiro BJ, Friedman J, Cordero OX, Preheim SP, Timberlake SC, Szabó G, et al. Population genomics of early events in the ecological differentiation of bacteria. Science. 2012;336:48–51.

  71. 71.

    Cadillo-Quiroz H, Didelot X, Held NL, Herrera A, Darling A, Reno ML, et al. Patterns of gene flow define species of thermophilic Archaea. PLoS Biol. 2012;10:e1001265.

  72. 72.

    Orsini L, Vanoverbeke J, Swillen I, Mergeay J, De Meester L. Drivers of population genetic differentiation in the wild: isolation by dispersal limitation, isolation by adaptation and isolation by colonization. Mol Ecol. 2013;22:5983–99.

  73. 73.

    Harvey PH, Pagel MD. The comparative method in evolutionary biology. Oxford, UK: Oxford University Press; 1991.

  74. 74.

    Losos JB. Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol Lett. 2008;11:995–1003.

  75. 75.

    Buckley LB, Davies TJ, Ackerly DD, Kraft NJB, Harrison SP, Anacker BL, et al. Phylogeny, niche conservatism and the latitudinal diversity gradient in mammals. Proc R Soc Lond Biol. 2010;277:2131–8.

  76. 76.

    Wiens JJ, Graham CH. Niche conservatism: integrating evolution, ecology, and conservation biology. Annu Rev Ecol Evol Syst. 2005;36:519–39.

  77. 77.

    Morinière J, Van Dam MH, Hawlitschek O, Bergsten J, Michat MC, Hendrich L, et al. Phylogenetic niche conservatism explains an inverse latitudinal diversity gradient in freshwater arthropods. Sci Rep 2016;6.26340.

  78. 78.

    Barberán A, Velazques HC, Jones S, Fierer N. Hiding in plain sight: mining bacterial species records for phenotypic trait information. mSphere. 2017;2:e00237–17.

  79. 79.

    Martiny AC, Treseder K, Pusch G. Phylogenetic conservatism of functional traits in microorganisms. ISME J. 2013;7:830–8.

  80. 80.

    Davis MB, Shaw RG. Range shifts and adaptive responses to Quaternary climate change. Science. 2001;292:673–9.

  81. 81.

    Cooper VS, Bennett AF, Lenski RE. Evolution of thermal dependence of growth rate of Escherichia coli populations during 20,000 generations in a constant environment. Evolution. 2001;55:889–96.

  82. 82.

    Bennett AF, Lenski RE, Mittler JE. Evolutionary adaptation to temperature. I. Fitness responses of Escherichia coli to changes in its thermal environment. Evolution. 1992;46:16–30.

  83. 83.

    Oliverio AM, Bradford MA, Fierer N. Identifying the microbial taxa that consistently respond to soil warming across time and space. Glob Chang Biol. 2017;23:2117–29.

  84. 84.

    Clayton L, Attig JW, Mickelson DM, Johnson MD, Syverson KM. Glaciation of Wisconsin. Wisconsin Geological and Natural History Survey. 2006;36:1–4

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Acknowledgements

We would like to thank Mary Jo Choudoir and Dunroven Farm for providing soil samples from northern Wisconsin. This material is based upon work supported by the National Science Foundation under grant no. DEB-1456821 awarded to Daniel H. Buckley.

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  1. School of Integrative Plant Science, Cornell University, Ithaca, NY, 14853, USA

    • Mallory J. Choudoir
    •  & Daniel H. Buckley
  2. University of Colorado Boulder, Boulder, CO, 80309, USA

    • Mallory J. Choudoir

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The authors declare that they have no conflict of interest.

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Correspondence to Daniel H. Buckley.

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https://doi.org/10.1038/s41396-018-0180-3