A globally ubiquitous symbiont can drive experimental host evolution.

Kieran A Bates, Jai S Bolton, Kayla C King
Author Information
  1. Kieran A Bates: Department of Zoology, University of Oxford, Oxford, UK. ORCID
  2. Jai S Bolton: Department of Zoology, University of Oxford, Oxford, UK.
  3. Kayla C King: Department of Zoology, University of Oxford, Oxford, UK.

Abstract

Organisms harbour myriad microbes which can be parasitic or protective against harm. The costs and benefits resulting from these symbiotic relationships can be context-dependent, but the evolutionary consequences to hosts of these transitions remain unclear. Here, we mapped the Leucobacter genus across 13,715 microbiome samples (163 studies) to reveal a global distribution as a free-living microbe or a symbiont of animals and plants. We showed that across geographically distant locations (South Africa, France, Cape Verde), Leucobacter isolates vary substantially in their virulence to an associated animal host, Caenorhabditis nematodes. We further found that multiple Leucobacter sequence variants co-occur in wild Caenorhabditis spp. which combined with natural variation in virulence provides real-world potential for Leucobacter community composition to influence host fitness. We examined this by competing C. elegans genotypes that differed in susceptibility to different Leucobacter species in an evolution experiment. One Leucobacter species was found to be host-protective against another, virulent parasitic species. We tested the impact of host genetic background and Leucobacter community composition on patterns of host-based defence evolution. We found host genotypes conferring defence against the parasitic species were maintained during infection. However, when hosts were protected during coinfection, host-based defences were nearly lost from the population. Overall, our results provide insight into the role of community context in shaping host evolution during symbioses.

Keywords

Associated Data

figshare | 10.6084/m9.figshare.c.5420061

References

  1. Ademola, I. O., & Odeniran, P. O. (2016). Co-infection with Plasmodium berghei and Trypanosoma brucei increases severity of malaria and trypanosomiasis in mice. Acta Tropica, 159, 29-35. https://doi.org/10.1016/j.actatropica.2016.03.030.
  2. Akman, L., Yamashita, A., Watanabe, H., Oshima, K., Shiba, T., Hattori, M., & Aksoy, S. (2002). Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nature Genetics, 32(3), 402-407. https://doi.org/10.1038/ng986
  3. Antonovics, J., & Thrall, P. H. (1994). Cost of resistance and the maintenance of genetic polymorphism in host-pathogen systems. Proceedings of the Royal Society B: Biological Sciences, 257, 105-110.
  4. Baker, D. M., Freeman, C. J., Wong, J. C. Y., Fogel, M. L., & Knowlton, N. (2018). Climate change promotes parasitism in a coral symbiosis. The ISME Journal, 12(3), 921-930. https://doi.org/10.1038/s41396-018-0046-8
  5. Bartlett, L. J., Wilfert, L., & Boots, M. (2018). A genotypic trade-off between constitutive resistance to viral infection and host growth rate. Evolution, 72(12), 2749-2757. https://doi.org/10.1111/evo.13623
  6. Bazzone, L. E., Smith, P. M., Rutitzky, L. I., Shainheit, M. G., Urban, J. F., Setiawan, T., Blum, A. M., Weinstock, J. V., & Stadecker, M. J. (2008). Coinfection with the intestinal nematode Heligmosomoides polygyrus markedly reduces hepatic egg-induced immunopathology and proinflammatory cytokines in mouse models of severe schistosomiasis. Infection and Immunity, 76(11), 5164-5172. https://doi.org/10.1128/IAI.00673-08
  7. Best, S. M., & Kerr, P. J. (2000). Coevolution of host and virus: The pathogenesis of virulent and attenuated strains of myxoma virus in resistant and susceptible European rabbits. Virology, 267(1), 36-48. https://doi.org/10.1006/viro.1999.0104
  8. Bonneaud, C., Tardy, L., Giraudeau, M., Hill, G. E., McGraw, K. J., & Wilson, A. J. (2019). Evolution of both host resistance and tolerance to an emerging bacterial pathogen. Evolution Letters, 3(5), 544-554. https://doi.org/10.1002/evl3.133
  9. Brucker, R. M., & Bordenstein, S. R. (2012). Speciation by symbiosis. Trends in Ecology & Evolution, 27(8), 443-451. https://doi.org/10.1016/j.tree.2012.03.011
  10. Brucker, R. M., & Bordenstein, S. R. (2013). The hologenomic basis of speciation: Gut bacteria cause hybrid lethality in the genus Nasonia. Science, 341(6146), 667-669. https://doi.org/10.1126/science.1240659
  11. Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A., & Holmes, S. P. (2016). DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods, 13(7), 581-583. https://doi.org/10.1038/nmeth.3869
  12. Clark, L. C., & Hodgkin, J. (2015). Leucobacter musarum subsp. musarum sp. nov., subsp. nov., Leucobacter musarum subsp. japonicus subsp. nov., and Leucobacter celer subsp. astrifaciens subsp. nov., three nematopathogenic bacteria isolated from Caenorhabditis, with an emended description of Leucobacter celer. International Journal of Systematic and Evolutionary Microbiology, 65(11), 3977-3984. http://dx.doi.org/10.1099/ijsem.0.000523
  13. Clay, K., Holah, J., & Rudgers, J. A. (2005). Herbivores cause a rapid increase in hereditary symbiosis and alter plant community composition. Proceedings of the National Academy of Sciences, 102(35), 12465-12470. https://doi.org/10.1073/pnas.0503059102
  14. Dirksen, P., Marsh, S. A., Braker, I., Heitland, N., Wagner, S., Nakad, R., Mader, S., Petersen, C., Kowallik, V., Rosenstiel, P., Félix, M.-A., & Schulenburg, H. (2016). The native microbiome of the nematode Caenorhabditis elegans: Gateway to a new host-microbiome model. BMC Biology, 14(1), 38. https://doi.org/10.1186/s12915-016-0258-1
  15. Drew, G. C., Stevens, E. J., & King, K. C. (2021). Microbial evolution and transitions along the parasite-mutualist continuum. Nature Reviews Microbiology, https://doi.org/10.1038/s41579-021-00550-7
  16. Eberl, L., & Vandamme, P. (2016). Members of the genus Burkholderia: Good and bad guys. F1000Research, 5, 1007. https://doi.org/10.12688/f1000research.8221.1
  17. Fisher, R. M., Henry, L. M., Cornwallis, C. K., Kiers, E. T., & West, S. A. (2017). The evolution of host-symbiont dependence. Nature Communications, 8(1), 15973. https://doi.org/10.1038/ncomms15973
  18. Ford, S. A., & King, K. C. (2021). In vivo microbial coevolution favors host protection and plastic downregulation of immunity. Molecular Biology and Evolution, 38(4), 1330-1338. https://doi.org/10.1093/molbev/msaa292
  19. Fraune, S., Anton-Erxleben, F., Augustin, R., Franzenburg, S., Knop, M., Schröder, K., Willoweit-Ohl, D., & Bosch, T. C. (2015). Bacteria-bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance. The ISME Journal, 9(7), 1543-1556. https://doi.org/10.1038/ismej.2014.239
  20. Gould, A. L., Zhang, V., Lamberti, L., Jones, E. W., Obadia, B., Korasidis, N., Gavryushkin, A., Carlson, J. M., Beerenwinkel, N., & Ludington, W. B. (2018). Microbiome interactions shape host fitness. Proceedings of the National Academy of Sciences, 115(51), E11951-E11960. https://doi.org/10.1073/pnas.1809349115
  21. Graham, A. L., Allen, J. E., & Read, A. F. (2005). Evolutionary causes and consequences of immunopathology. Annual Review of Ecology, Evolution, and Systematics, 36(1), 373-397. https://doi.org/10.1146/annurev.ecolsys.36.102003.152622
  22. Haine, E. R. (2008). Symbiont-mediated protection. Proceedings of the Royal Society B: Biological Sciences, 275(1633), 353-361. https://doi.org/10.1098/rspb.2007.1211
  23. Hartl, D. L., & Clark, A. G. (1997). Principles of population genetics. Sinaner.
  24. Hodgkin, J., Coulson, A., & Kuwabara, P. (2001). Mapping useful GFP insertions; evidence for local suppression of recombination. Worm Breeder’s Gazette, 16(5), 20.
  25. Hodgkin, J., Félix, M.-A., Clark, L. C., Stroud, D., & Gravato-Nobre, M. J. (2013). Two Leucobacter strains exert complementary virulence on Caenorhabditis including death by worm-star formation. Current Biology, 23(21), 2157-2161. https://doi.org/10.1016/j.cub.2013.08.060
  26. Holt, C. C., van der Giezen, M., Daniels, C. L., Stentiford, G. D., & Bass, D. (2020). Spatial and temporal axes impact ecology of the gut microbiome in juvenile European lobster (Homarus gammarus). The ISME Journal, 14(2), 531-543. https://doi.org/10.1038/s41396-019-0546-1
  27. Hosokawa, T., Koga, R., Kikuchi, Y., Meng, X.-Y., & Fukatsu, T. (2010). Wolbachia as a bacteriocyte-associated nutritional mutualist. Proceedings of the National Academy of Sciences, 107(2), 769-774. https://doi.org/10.1073/pnas.0911476107
  28. Hothorn, T., Bretz, F., & Westfall, P. (2008). Simultaneous inference in general parametric models. Biometrical Journal, 50(3), 346-363. https://doi.org/10.1002/bimj.200810425
  29. Hrček, J., Parker, B. J., McLean, A. H. C., Simon, J.-C., Mann, C. M., & Godfray, H. C. J. (2018). Hosts do not simply outsource pathogen resistance to protective symbionts. Evolution, 72(7), 1488-1499. https://doi.org/10.1111/evo.13512
  30. Jaenike, J., Unckless, R., Cockburn, S. N., Boelio, L. M., & Perlman, S. J. (2010). Adaptation via symbiosis: Recent spread of a Drosophila defensive symbiont. Science, 329(5988), 212-215. https://doi.org/10.1126/science.1188235
  31. Johnke, J., Dirksen, P., & Schulenburg, H. (2020). Community assembly of the native C. elegans microbiome is influenced by time, substrate and individual bacterial taxa. Environmental Microbiology, 22(4), 1265-1279. https://doi.org/10.1111/1462-2920.14932
  32. Johnston, P. R., & Rolff, J. (2015). Host and symbiont jointly control gut microbiota during complete metamorphosis. PLoS Path, 11(11), e1005246. https://doi.org/10.1371/journal.ppat.1005246
  33. Jones, B. W., & Nishiguchi, M. K. (2004). Counterillumination in the Hawaiian bobtail squid, Euprymna scolopes Berry (Mollusca: Cephalopoda). Marine Biology, 144(6), 1151-1155. https://doi.org/10.1007/s00227-003-1285-3
  34. Kerr, P. J., & Best, S. M. (1998). Myxoma virus in rabbits. Revue Scientifique Et Technique De l’OIE, 17(1), 256-268. https://doi.org/10.20506/rst.17.1.1081
  35. Khojandi, N., Haselkorn, T. S., Eschbach, M. N., Naser, R. A., & DiSalvo, S. (2019). Intracellular Burkholderia symbionts induce extracellular secondary infections; driving diverse host outcomes that vary by genotype and environment. The ISME Journal, 13(8), 2068-2081. https://doi.org/10.1038/s41396-019-0419-7
  36. King, K. C. (2019). Defensive symbionts. Current Biology, 29(3), R78-R80. https://doi.org/10.1016/j.cub.2018.11.028
  37. King, K. C., Brockhurst, M. A., Vasieva, O., Paterson, S., Betts, A., Ford, S. A., Frost, C. L., Horsburgh, M. J., Haldenby, S., & Hurst, G. D. (2016). Rapid evolution of microbe-mediated protection against pathogens in a worm host. The ISME Journal, 10(8), 1915-1924. https://doi.org/10.1038/ismej.2015.259
  38. Kosmidis, I., & Firth, D. (2021). Jeffreys-prior penalty, finiteness and shrinkage in binomial-response generalized linear models. Biometrika, 108(1), 71-82. https://doi.org/10.1093/biomet/asaa052
  39. Kraaijeveld, A. R., & Godfray, H. C. J. (1997). Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature, 389(6648), 278-280. https://doi.org/10.1038/38483
  40. Laine, A.-L. (2006). Evolution of host resistance: Looking for coevolutionary hotspots at small spatial scales. Proceedings of the Royal Society B: Biological Sciences, 273(1584), 267-273. https://doi.org/10.1098/rspb.2005.3303
  41. Leclair, M., Polin, S., Jousseaume, T., Simon, J.-C., Sugio, A., Morlière, S., Fukatsu, T., Tsuchida, T., & Outreman, Y. (2017). Consequences of coinfection with protective symbionts on the host phenotype and symbiont titres in the pea aphid system. Insect Science, 24(5), 798-808. https://doi.org/10.1111/1744-7917.12380
  42. Lloyd-Smith, J. O., Schreiber, S. J., Kopp, P. E., & Getz, W. M. (2005). Superspreading and the effect of individual variation on disease emergence. Nature, 438(7066), 355-359. https://doi.org/10.1038/nature04153
  43. Lochmiller, R. L., & Deerenberg, C. (2000). Trade-offs in evolutionary immunology: Just what is the cost of immunity? Oikos, 88(1), 87-98. https://doi.org/10.1034/j.1600-0706.2000.880110.x
  44. Luong, L. T., & Polak, M. (2007). Costs of resistance in the Drosophila macrocheles system: A negative correlation between ectoparasite resistance and reproduction. Evolution, 61(6), 1391-1402. https://doi.org/10.1111/j.1558-5646.2007.00116.x
  45. Martinez, J., Cogni, R., Cao, C., Smith, S., Illingworth, C. J. R., & Jiggins, F. M. (2016). Addicted? Reduced host resistance in populations with defensive symbionts. Proceedings of the Royal Society B: Biological Sciences, 283(1833), 20160778. https://doi.org/10.1098/rspb.2016.0778
  46. McDonald, D., Kaehler, B., Gonzalez, A., DeReus, J., Ackermann, G., Marotz, C., Huttley, G., & Knight, R. (2019). redbiom: A rapid sample discovery and feature characterization system. mSystems, 4(4), https://doi.org/10.1128/mSystems.00215-19
  47. McKean, K. A., Yourth, C. P., Lazzaro, B. P., & Clark, A. G. (2008). The evolutionary costs of immunological maintenance and deployment. BMC Evolutionary Biology, 8(1), 76. https://doi.org/10.1186/1471-2148-8-76
  48. McMurdie, P. J., & Holmes, S. (2013). phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One, 8(4), e61217. https://doi.org/10.1371/journal.pone.0061217
  49. Metcalf, C. J. E., & Koskella, B. (2019). Protective microbiomes can limit the evolution of host pathogen defense. Evolution Letters, 3(5), 534-543. https://doi.org/10.1002/evl3.140
  50. Muir, R. E., & Tan, M.-W. (2008). Virulence of Leucobacter chromiireducens subsp. solipictus to Caenorhabditis elegans: Characterization of a novel host-pathogen Interaction. Applied and Environmental Microbiology, 74(13), 4185-4198. https://doi.org/10.1128/AEM.00381-08
  51. Murfin, K. E., Ginete, D. R., Bashey, F., & Goodrich-Blair, H. (2019). Symbiont-mediated competition: Xenorhabdus bovienii confer an advantage to their nematode host Steinernema affine by killing competitor Steinernema feltiae. Environmental Microbiology, 21(9), 3229-3243. https://doi.org/10.1111/1462-2920.14278
  52. Oliver, K. M., Campos, J., Moran, N. A., & Hunter, M. S. (2008). Population dynamics of defensive symbionts in aphids. Proceedings of the Royal Society B: Biological Sciences, 275(1632), 293-299. https://doi.org/10.1098/rspb.2007.1192
  53. Park, T. (1948). Interspecies competition in populations of Trilobium confusum Duval and Trilobium castaneum Herbst. Ecological Monographs, 18(2), 265-307. https://doi.org/10.2307/1948641
  54. Parker, B. J., Hrček, J., McLean, A. H. C., & Godfray, H. C. J. (2017). Genotype specificity among hosts, pathogens, and beneficial microbes influences the strength of symbiont-mediated protection. Evolution, 71(5), 1222-1231. https://doi.org/10.1111/evo.13216
  55. Penley, M. J., Greenberg, A. B., Khalid, A., Namburar, S. R., & Morran, L. T. (2018). No measurable fitness cost to experimentally evolved host defence in the Caenorhabditis elegans-Serratia marcescens host-parasite system. Journal of Evolutionary Biology, 31(12), 1976-1981. https://doi.org/10.1111/jeb.13372
  56. Percudani, R. (2013). A microbial metagenome (Leucobacter sp.) in Caenorhabditis whole genome sequences. Bioinformatics and Biology Insights, 7, BBI.S11064. https://doi.org/10.4137/BBI.S11064
  57. Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., & Glöckner, F. O. (2012). The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research, 41(D1), D590-D596. https://doi.org/10.1093/nar/gks1219
  58. Rafaluk-Mohr, C., Ashby, B., Dahan, D. A., & King, K. C. (2018). Mutual fitness benefits arise during coevolution in a nematode-defensive microbe model. Evolution Letters, 2(3), 246-256. https://doi.org/10.1002/evl3.58
  59. Rudolf, V. H. W., & Antonovics, J. (2005). Species coexistence and pathogens with frequency-dependent transmission. The American Naturalist, 166(1), 112-118. https://doi.org/10.1086/430674
  60. Samuel, B. S., Rowedder, H., Braendle, C., Félix, M.-A., & Ruvkun, G. (2016). Caenorhabditis elegans responses to bacteria from its natural habitats. Proceedings of the National Academy of Sciences, 113(27), E3941-E3949. https://doi.org/10.1073/pnas.1607183113
  61. Schmid-Hempel, P. (2003). Variation in immune defence as a question of evolutionary ecology. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270(1513), 357-366. https://doi.org/10.1098/rspb.2002.2265
  62. Schwenke, R. A., Lazzaro, B. P., & Wolfner, M. F. (2016). Reproduction-immunity trade-offs in insects. Annual Review of Entomology, 61(1), 239-256. https://doi.org/10.1146/annurev-ento-010715-023924
  63. Shapira, M. (2016). Gut microbiotas and host evolution: Scaling up symbiosis. Trends in Ecology & Evolution, 31(7), 539-549. https://doi.org/10.1016/j.tree.2016.03.006
  64. Sharon, G., Segal, D., Ringo, J. M., Hefetz, A., Zilber-Rosenberg, I., & Rosenberg, E. (2010). Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proceedings of the National Academy of Sciences, 107(46), 20051-20056. https://doi.org/10.1073/pnas.1009906107
  65. Smith, A. H., Łukasik, P., O’Connor, M. P., Lee, A., Mayo, G., Drott, M. T., Doll, S., Tuttle, R., Disciullo, R. A., Messina, A., Oliver, K. M., & Russell, J. A. (2015). Patterns, causes and consequences of defensive microbiome dynamics across multiple scales. Molecular Ecology, 24(5), 1135-1149. https://doi.org/10.1111/mec.13095
  66. Somvanshi, V. S., Lang, E., Schumann, P., Pukall, R., Kroppenstedt, R. M., Ganguly, S., & Stackebrandt, E. (2007). Leucobacter iarius sp. nov., in the family Microbacteriaceae. International Journal of Systematic and Evolutionary Microbiology, 57(4), 682-686. https://doi.org/10.1099/ijs.0.64683-0
  67. Stein, R. A. (2011). Super-spreaders in infectious diseases. International Journal of Infectious Diseases, 15(8), e510-e513. https://doi.org/10.1016/j.ijid.2010.06.020
  68. Stiernagle, T. (2006). Maintenance of C. elegans. WormBook, https://doi.org/10.1895/wormbook.1.101.1
  69. Thompson, L. R., Sanders, J. G., McDonald, D., Amir, A., Ladau, J., Locey, K. J., Prill, R. J., Tripathi, A., Gibbons, S. M., Ackermann, G., Navas-Molina, J. A., Janssen, S., Kopylova, E., Vázquez-Baeza, Y., González, A., Morton, J. T., Mirarab, S., Zech Xu, Z., Jiang, L., … Knight, R. (2017). A communal catalogue reveals Earth’s multiscale microbial diversity. Nature, 551(7681), 457-463. https://doi.org/10.1038/nature24621
  70. Tianero, M. D. B., Kwan, J. C., Wyche, T. P., Presson, A. P., Koch, M., Barrows, L. R., Bugni, T. S., & Schmidt, E. W. (2015). Species specificity of symbiosis and secondary metabolism in ascidians. The ISME Journal, 9(3), 615-628. https://doi.org/10.1038/ismej.2014.152
  71. Vorburger, C., & Gouskov, A. (2011). Only helpful when required: A longevity cost of harbouring defensive symbionts. Journal of Evolutionary Biology, 24(7), 1611-1617. https://doi.org/10.1111/j.1420-9101.2011.02292.x
  72. Walterson, A. M., & Stavrinides, J. (2015). Pantoea: Insights into a highly versatile and diverse genus within the Enterobacteriaceae. FEMS Microbiology Reviews, 39(6), 968-984. https://doi.org/10.1093/femsre/fuv027
  73. Wang, Q., Garrity, G. M., Tiedje, J. M., & Cole, J. R. (2007). Naive bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16), 5261-5267. https://doi.org/10.1128/AEM.00062-07
  74. Weldon, S. R., Russell, J. A., & Oliver, K. M. (2019). More is not always better: Coinfections with defensive symbionts generate highly variable outcomes. Applied and Environmental Microbiology, 86(5), https://doi.org/10.1128/AEM.02537-19
  75. Wollenberg, M. S., & Ruby, E. G. (2012). Phylogeny and fitness of Vibrio fischeri from the light organs of Euprymna scolopes in two Oahu, Hawaii populations. The ISME Journal, 6(2), 352-362. https://doi.org/10.1038/ismej.2011.92
  76. Zbinden, M., Haag, C. R., & Ebert, D. (2008). Experimental evolution of field populations of Daphnia magna in response to parasite treatment. Journal of Evolutionary Biology, 21(4), 1068-1078. https://doi.org/10.1111/j.1420-9101.2008.01541.x

Grants

  1. BB/M011224/1/Biotechnology and Biological Sciences Research Council

MeSH Term

Animals
Caenorhabditis elegans
Microbiota
Nematoda
Parasites
Symbiosis

Word Cloud

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