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Primitive agriculture in a social amoeba

Nature volume 469, pages 393–396 (2011)Cite this article

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Abstract

Agriculture has been a large part of the ecological success of humans1. A handful of animals, notably the fungus-growing ants, termites and ambrosia beetles2,3,4, have advanced agriculture that involves dispersal and seeding of food propagules, cultivation of the crop and sustainable harvesting5. More primitive examples, which could be called husbandry because they involve fewer adaptations, include marine snails farming intertidal fungi6 and damselfish farming algae7. Recent work has shown that microorganisms are surprisingly like animals in having sophisticated behaviours such as cooperation, communication8,9 and recognition10,11, as well as many kinds of symbiosis12,13,14,15. Here we show that the social amoeba Dictyostelium discoideum has a primitive farming symbiosis that includes dispersal and prudent harvesting of the crop. About one-third of wild-collected clones engage in husbandry of bacteria. Instead of consuming all bacteria in their patch, they stop feeding early and incorporate bacteria into their fruiting bodies. They then carry bacteria during spore dispersal and can seed a new food crop, which is a major advantage if edible bacteria are lacking at the new site. However, if they arrive at sites already containing appropriate bacteria, the costs of early feeding cessation are not compensated for, which may account for the dichotomous nature of this farming symbiosis. The striking convergent evolution between bacterial husbandry in social amoebas and fungus farming in social insects makes sense because multigenerational benefits of farming go to already established kin groups.

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Figure 1: Fruiting body structure and sorus contents from farmer and non-farmer D.discoideum clones.
Figure 2: Farmers readily reassociate with bacteria, suggesting a persistent interaction.
Figure 3: The advantage of carrying food is context dependent.
Figure 4: Life-history traits differ between farmers and non-farmers.

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References

  1. Smith, B. D. (ed.) The Emergence of Agriculture (Scientific American Library, Freeman, 1995)

    Google Scholar 

  2. Aanen, D. et al. The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proc. Natl Acad. Sci. USA 99, 14887–14892 (2002)

    Article  ADS  CAS  Google Scholar 

  3. Farrell, B. et al. The evolution of agriculture in beetles (Curculionidae: Scolytinae and Platypodinae). Evolution 55, 2011–2027 (2001)

    Article  CAS  Google Scholar 

  4. Mueller, U. G., Schultz, T., Currie, C., Adams, R. & Malloch, D. The origin of the ant-fungus mutualism. Q. Rev. Biol. 76, 169–197 (2001)

    Article  CAS  Google Scholar 

  5. Mueller, U. G., Gerardo, N. M., Aanen, D. K., Six, D. L. & Schultz, T. R. The evolution of agriculture in insects. Annu. Rev. Ecol. Evol. Syst. 36, 563–595 (2005)

    Article  Google Scholar 

  6. Silliman, B. R. & Newell, S. Y. Fungal farming in a snail. Proc. Natl Acad. Sci. USA 100, 15643–15648 (2003)

    Article  ADS  CAS  Google Scholar 

  7. Hata, H. & Kato, M. A novel obligate cultivation mutualism between damselfish and Polysiphonia algae. Biol. Lett. 2, 593–596 (2006)

    Article  Google Scholar 

  8. Crespi, B. J. The evolution of social behavior in microorganisms. Trends Ecol. Evol. 16, 178–183 (2001)

    Article  Google Scholar 

  9. Keller, L. & Surette, M. G. Communication in bacteria: an ecological and evolutionary perspective. Nature Rev. Microbiol. 4, 249–258 (2006)

    Article  CAS  Google Scholar 

  10. Mehdiabadi, N. J. et al. Kin preference in a social amoeba. Nature 442, 881–882 (2006)

    Article  ADS  CAS  Google Scholar 

  11. Ostrowski, E. A., Katoh, M., Shaulsky, G., Queller, D. C. & Strassmann, J. E. Kin discrimination increases with genetic distance in a social amoeba. PLoS Biol. 6, e287 (2008)

    Article  Google Scholar 

  12. Douglas, A. E. Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera . Annu. Rev. Entomol. 43, 17–37 (1998)

    Article  CAS  Google Scholar 

  13. Moran, N. A., Dunbar, H. E. & Wilcox, J. L. Regulation of transcription in a reduced bacterial genome: nutrient-provisioning genes of the obligate symbiont Buchnera aphidicola. J. Bacteriol. 187, 4229–4237 (2005)

    Article  CAS  Google Scholar 

  14. Bäckhed, F., Ley, R. E., Sonnenburg, J. L., Peterson, D. A. & Gordon, J. I. Host-bacterial mutualism in the human intestine. Science 307, 1915–1920 (2005)

    Article  ADS  Google Scholar 

  15. Sears, C. L. A dynamic partnership: celebrating our gut flora. Anaerobe 11, 247–251 (2005)

    Article  Google Scholar 

  16. Raper, K. B. The Dictyostelids 87–177 (Princeton Univ. Press, 1984)

    Book  Google Scholar 

  17. Kessin, R. H. Dictyostelium: Evolution, Cell Biology, and the Development of Multicellularity (Cambridge Univ. Press, 2001)

    Book  Google Scholar 

  18. Raper, K. B. Growth and development of Dictyostelium discoideum with different bacterial associates. J. Agric. Res. 55, 289–316 (1937)

    Google Scholar 

  19. Matz, C. & Kjelleberg, S. Off the hook - how bacteria survive protozoan grazing. Trends Microbiol. 13, 302–307 (2005)

    Article  CAS  Google Scholar 

  20. Nadson, G. A. Des cultures du Dictyostelium mucoroides Bref. et des cultures pures des amibes en general. Scripta Bot. Horti Univ. Imp. Petropolitanae 15, 188–190 (1899)

    Google Scholar 

  21. Skupienski, F. X. Recherches sur le Cycle Evolutif de Certains Myxomycetes. PhD thesis, l’Universite de Paris. (1920)

    Google Scholar 

  22. Flowers, J. M. et al. Variation, sex, and social cooperation: molecular population genetics of the social amoeba Dictyostelium discoideum . PLoS Genet. 6, e1001013 (2010)

    Article  Google Scholar 

  23. Clark, F. in Soil Biology (eds Burges, A. & Raw, F. ) Ch. 2, 15–49 (Academic, 1967)

    Google Scholar 

  24. Heijnen, C. E., Burgers, S. & Vanveen, J. A. Metabolic activity and population dynamics of rhizobia introduced into unamended and bentonite-amended loamy sand. Appl. Environ. Microbiol. 59, 743–747 (1993)

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Horn, E. G. Food competition among the cellular slime molds (Acrasiae). Ecology 52, 475–484 (1971)

    Article  Google Scholar 

  26. Foster, K. R., Shaulsky, G., Strassmann, J. E., Queller, D. C. & Thompson, C. R. L. Pleiotropy as a mechanism to stabilize cooperation. Nature 431, 693–696 (2004)

    Article  ADS  CAS  Google Scholar 

  27. Gilbert, O. M., Foster, K. R., Mehdiabadi, N. J., Strassmann, J. E. & Queller, D. C. High relatedness maintains multicellular cooperation in a social amoeba by controlling cheater mutants. Proc. Natl Acad. Sci. USA 104, 8913–8917 (2007)

    Article  ADS  CAS  Google Scholar 

  28. Santorelli, L. A. et al. Facultative cheater mutants reveal the genetic complexity of cooperation in social amoebae. Nature 451, 1107–1110 (2008)

    Article  ADS  CAS  Google Scholar 

  29. Benabentos, R. et al. Polymorphic members of the lag gene family mediate kin discrimination in Dictyostelium . Curr. Biol. 19, 567–572 (2009)

    Article  CAS  Google Scholar 

  30. Fortunato, A., Strassmann, J. E., Santorelli, L. & Queller, D. C. Co-occurrence in nature of different clones of the social amoeba, Dictyostelium discoideum. Mol. Ecol. 12, 1031–1038 (2003)

    Article  CAS  Google Scholar 

  31. Huelsenbeck, J. P. & Ronquist, F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755 (2001)

    Article  CAS  Google Scholar 

  32. Tamura, K., Dudley, J., Nei, M. & Kumar, S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596–1599 (2007)

    Article  CAS  Google Scholar 

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Acknowledgements

We thank J. Rudgers, G. Saxer Quance, L. Campbell, E. Ostrowski, O. Gilbert, A. Savage, J. Ahern, K. Crawford, S. Chamberlain, S. Read, D. Nguyen, K. Foster, H. Kaplan, D. Hatton and K. Boomsma for discussions and advice. This material is based on work supported by the US National Science Foundation.

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Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, Rice University, 6100 Main Street, Houston, 77005, Texas, USA

    Debra A. Brock, Tracy E. Douglas, David C. Queller & Joan E. Strassmann

Authors
  1. Debra A. Brock
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  2. Tracy E. Douglas
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  3. David C. Queller
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  4. Joan E. Strassmann
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Contributions

D.A.B. identified the symbiosis, performed the experiments and analysed the data. T.E.D. constructed and analysed the phylogeny. D.A.B., T.E.D., D.C.Q. and J.E.S. designed the experiments, discussed the results and wrote the manuscript.

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Correspondence to Debra A. Brock.

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The authors declare no competing financial interests.

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Brock, D., Douglas, T., Queller, D. et al. Primitive agriculture in a social amoeba. Nature 469, 393–396 (2011). https://doi.org/10.1038/nature09668

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  1. Edward Mitchell

    Primitive agriculture in a social amoeba : more than meets the eye?

    Brock et al. 1 presented some interesting and intruiging results on the primitive farming symbiosis of the Dictyostelium discoideum.
    This new form of symbiosis adds to the many existing symbiotic associations involving protists and bacteria including endosymbionts such as mitochondia, chloroplasts, symbiotic algae, or bacteria such as chlamydiae, Rickettsia etc.
    An interesting observation of Brock et al. is that the amoebae carried a variety of bacterial species, about half of which serve as food source while the function of the other half is not clear. Brock et al. did not explore this aspect in detail but suggest that there is no close relationship between the amoeba and the bacteria. This apparently rules out the possibility for co-evolution between the amoeba and the bacteria. Farmers and non-farmers Dictyostelium are fundamentally different in their behaviour but apparently this does not imply that their preys are different or that they were selected or otherwise modified though the symbiotic relationship with the amoeba.
    The apparent lack of association between Dictyostelium and farmed bacteria could be due to the fact that farmers grow a set of bacteria but that, as Brock et al. noted, only some of these were recorded and obtaining a full list of cultivated bacteria was beyond their goal. Given that most soil microorganisms cannot be grown in typical laboratory conditions, it is possible that not all strains transported by the farmer amoebae could develop, either because of unsuited growth medium, or because of inter-strain competition on the agar. However, we believe that this interesting association deserves to be studied further and we provide here some hypotheses to be tested.
    Growing several bacterial species would be beneficial to the amoebae because it would increase the likelihood that at least one bacterial species could grow on the newly colonised environment. Some bacteria would thus grow and feed the new amoeba clone, regardless of the characteristics of the environment where the spore falls. Such a strategy would be analogous to farmers travelling to new land and carrying with them a variety of seeds (e.g. European settlers in North-America) adapted to different soil conditions and climates. It would be interesting to assess if the amoebae carry with them a diverse assemblage of bacteria over several generations even if some of these are only rarely beneficial to them. This « insurance hypothesis » would be quite easy to test using alternating substrates and growth conditions.
    A second avenue to explore is that of a possible selection of bacteria by the amoeba. Indeed it would be plausible to imagine that the amoeba recognizes the bacteria species that are « cultivable » and therefore preferentially selects some species over others. This would in turn make it likely that the relationship between the amoeba and these bacteria are rather tight, indeed corresponding to a form of mutually beneficial symbiosis ; the benefit to the amoeba was established in the study of Brock et al. The benefit to the bacteria is the transport to new habitat. In such a relationship, one can expect â&#x80&#x9cartificialâ&#x80&#x9d selection of the amoeba on the bacteria, analogous to the artificial selection of plants and animals by Human farmers.
    Finally, symbioses between micro organisms most often lead to horizontal gene transfer. One could thus expect mutual lateral transfer of genes to occur, especially if the relationship between the amoeba and the bacteria is a lasting one. If this was demonstrated it would provide not only evidence for extremely ancient « agriculture », but also for ancient genetic modification of cultivated organisms, in other words : « ancient GMOs »!

    Edward Mitchell & Enrique Lara
    Laboratory of Soil Biology, University of Neuchâtel, Switzerland

    References
    1&#009Brock, D. A., Douglas, T. E., Queller, D. C. & Strassmann, J. E. Primitive agriculture in a social amoeba. Nature 469, 393-396, doi:10.1038/nature09668 (2011).

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