From competition to cooperation: Paradigm shifts in trait-based ecology change our understanding of the processes that structure microbial communities

Authors

  • Claudia Piccini Laboratorio de Ecología Microbiana Acuática, Departamento de Microbiología, Instituto de Investigaciones Biológicas Clemente Estable. Montevideo, Uruguay
  • Melina Devercelli Instituto Nacional de Limnología, INALI (CONICET-UNL); Instituto Nacional del Agua, Subgerencia Centro Regional Litoral, SCRL-INA; Instituto Universitario de Seguridad Marítima, Prefectura Naval Argentina, IUSM-PNA, Argentina https://orcid.org/0000-0002-0464-2997
  • Lilen Yema Laboratorio de Limnología, IEGEBA (UBA-CONICET) https://orcid.org/0000-0002-9166-1378
  • Angel Segura MEDIA, Centro Universitario Regional Este, Universidad de la República, Uruguay https://orcid.org/0000-0002-1989-8899
  • Marcela Bastidas Navarro Laboratorio de Limnología, INIBIOMA (CONICET-Universidad Nacional del Comahue). Bariloche, Argentina https://orcid.org/0000-0002-6558-0451
  • María B. Sathicq Instituto de Limnología “Dr. Raúl A. Ringuelet”, ILPLA (UNLP-CONICET). Buenos Aires, Argentina
  • Gabriela Martínez de la Escalera Laboratorio de Ecología Microbiana Acuática, Departamento de Microbiología, Instituto de Investigaciones Biológicas Clemente Estable. Montevideo, Uruguay https://orcid.org/0000-0001-8240-0777
  • Ana Martínez Goicoechea Laboratorio de Fitoplancton Tóxico, DINARA. Ecología Funcional de sistemas acuáticos, CURE https://orcid.org/0000-0003-0596-7862
  • Mariana Rodrigues Amaral Da Costa Departamento de Ecologia Pós Graduação em Ecologia Universidade Federal do Rio Grande do Norte (UFRN), Brasil
  • Inés O'Farrell Laboratorio de Limnología, IEGEBA (UBA-CONICET) https://orcid.org/0000-0002-2236-2905
  • Enrique Lara Real Jardín Botánico-CSIC. Madrid, España
  • Carla Kruk IECA, Facultad de Ciencias, Universidad de la República, Uruguay. MEDIA, Centro Universitario Regional Este, Universidad de la República, Uruguay https://orcid.org/0000-0003-0760-1186

DOI:

https://doi.org/10.25260/EA.23.33.3.0.2093

Keywords:

traits, ecological theory, cooperation, competition, biases

Abstract

Prevailing social, economic and political ideas and paradigms constitute the lens through which scientists observe, assess, and understand the world. This affects how we interpret and understand the mechanisms governing the interaction between organisms and has led, in most cases, to dominant explanations and paradigms that are difficult to overthrow. This is the case of ecological theory, whose perspectives have followed the rationale of societal changes. From the industrial revolution to very recently, species competition for resources was regarded as one of the main drivers of species interactions. Nowadays, a new and rapidly growing way of thinking emerged, fueled by the high sequencing capacities, ultra-resolution microscopy and the slowly growing number of different social and gender perspectives participating in ecological studies: that living beings are not just single organisms interacting with other single organisms, but complex communities of macro- and microorganisms living and evolving together. The information emerging from this field is bringing new light to previously disregarded aspects of the ecological interactions that, in our opinion, will change the main paradigms in ecology. As members of a South American scientific network of Aquatic Microbial Ecology (MicroSudAqua), here we propose to explore alternative explanations for ecological observations, searching for new traits accounting for cooperation between microorganisms as a fundamental evolutionary and ecological strategy.

* Photo: Hyalosphenia papilio (Amoebozoa; Arcellinida), an amoeba species that hosts endosymbiotic algae related to the genus Chlorella. These organisms live in boreal peat bogs, an oligotrophic environment where they obtain much needed nutrients through their photosynthesizing partners. The amoeba requires the alga to close its life cycle, and has never been observed without it. Image: Prof. Edward A. D. Mitchell

References

Baedke, J., A. Fábregas-Tejeda, and A. Nieves Delgado. 2020. The holobiont concept before Margulis. J Exp Zool Part B Mol Dev Evol 334:149-155. https://doi.org/10.1002/jez.b.22931.

Baker, A. C. 2003. Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661-689. https://doi.org/10.1146/annurev.ecolsys.34.011802.132417.

Bell, W., and R. Mitchell. 1972. Chemotactic and growth responses of marine bacteria to algal extracellular products. The Biological Bulletin 143(2):265-277. https://doi.org/10.2307/1540052.

Bjorbækmo, M. F. M., A. Evenstad, L. L. Røsæg, A.K. Krabberød, and R. Logares. 2020. The planktonic protist interactome: where do we stand after a century of research? ISME J 14:544-559. https://doi.org/10.1038/s41396-019-0542-5.

Blackwell, A. L. 1875. The sexes throughout nature. GP Putnam's Sons.

Bordenstein, S. R., and K. R. Theis. 2015. Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLoS Biol 13:e1002226. https://doi.org/10.1371/journal.pbio.1002226.

Bosch, T. C. G., and D. J. Miller. 2016. The holobiont imperative. Perspectives from Early Emerging Animals. Vienna Springer. Pp. 155. https://doi.org/10.1007/978-3-7091-1896-2.

Butler, J. 2002. Gender trouble. Routledge. https://doi.org/10.4324/9780203902752.

Cohen, I. R., and A. Marron. 2020. The evolution of universal adaptations of life is driven by universal properties of matter: energy, entropy, and interaction. F1000Res. 2020 Jun 18;9:626. https://doi.org/10.12688/f1000research.24447.3.

Covich, A. 1972. Ecological economics of seed consumption by Peromyscus: a graphical model of resource substitution. Trans Connect Acad Arts Sci 44:71-93.

Darwin, C. R. 1859. On the origin of species by means of natural selection, or, The preservation of favoured races in the struggle for life. London: J. Murray, 1859. https://doi.org/10.5962/bhl.title.82303.

Donlan, R. M. 2002. Biofilms: microbial life on surfaces. Emerg Infect Dis 8(9):881-90. https://doi.org/10.3201/eid0809.020063.

Fort, H., and A. Segura. 2018. Competition across diverse taxa: quantitative integration of theory and empirical research using global indices of competition. Oikos 127(3):392-402. https://doi.org/10.1111/oik.04756.

Fu, H., M. Uchimiya, J. Gore, and M. A. Moran. 2020. Ecological drivers of bacterial community assembly in synthetic phycospheres. Proceedings of the National Academy of Sciences 117(7):3656-3662. https://doi.org/10.1073/pnas.1917265117.

Gause, G. F. 1934. The Struggle for Existence. Williams and Wilkins, Baltimore. https://doi.org/10.5962/bhl.title.4489.

Gayon, J. 1998. Darwinism’s struggle for survival: heredity and the hypothesis of natural selection. Cambridge University Press.

Gilbert, S. F., J. Sapp, and A. I. Tauber. 2012. A symbiotic view of life: we have never been individuals. The Quarterly Review of Biology 87(4):325-341. https://doi.org/10.1086/668166.

Goodwin, R. M. 1967. A growth cycle, in capitalism and growth. C. Feinstein (ed.).

Gordon, J., N. Knowlton, D. A. Relman, F. Rohwer, and M. Youle. 2013. Superorganisms and holobionts. Microbe 8:152-153. https://doi.org/10.1128/microbe.8.152.1.

Gould, S. 1981. The Mismeasure of Man. W. W. Norton and Company.

Grilli, J. 2020. Macroecological laws describe variation and diversity in microbial communities. Nature Communications 11(1):4743. https://doi.org/10.1038/s41467-020-18529-y.

Guerrero, R., L. Margulis, and M. Berlanga. 2013. Symbiogenesis: the holobiont as a unit of evolution. Int Microbiol 16:133-143.

Haraway, D. 1988. Situated Knowledges: The Science Question in Feminism and the Privilege of Partial Perspective. Feminist Studies 14(3):575-599. https://doi.org/10.2307/3178066.

Haraway, D. J. 2016. Staying with the trouble: Making kin in the Chthulucene. Duke University. https://doi.org/10.2307/j.ctv11cw25q.

Hodgson, J. G. E. A. 1999. Allocating C-S-R plant functional types: a soft approach to a hard problem. Oikos 85:282-294. https://doi.org/10.2307/3546494.

Jackrel, S. L., K. C. Schmidt, B. J. Cardinale, and V. J. Denef. 2020. Microbiomes reduce their host’s sensitivity to interspecific interactions. MBio 11:e02657-19. https://doi.org/10.1128/mBio.02657-19.

Jackrel, S. L., J. W. Yang, K. C. Schmidt, and V. J. Denef. 2021. Host specificity of microbiome assembly and its fitness effects in phytoplankton. ISME J 15:774-788. https://doi.org/10.1038/s41396-020-00812-x.

Kirk, G. 1997. Standing on solid ground: A materialist ecological feminism. In Materialist feminism: A reader in class, difference, and women’s lives. Psychology Press, New York: Routledge.

Krause, S., X. Le Roux, P. A. Niklaus, P. M. Van Bodegom, J. T. Lennon, et al. 2014. Trait-based approaches for understanding microbial biodiversity and ecosystem functioning. Frontiers in Microbiology 5:251. https://doi.org/10.3389/fmicb.2014.00251.

Law, R., and A. R. Watkinson. 1989. Competition. Ecological Concepts. Pp. 243-284 in J. M. Cherrett (ed.). Ecological Concepts. Blackwell Scientific, London.

Liu, H., T. G. Stephens, R. A. González-Pech, B. H. Beltrán, B. Lapeyre, P. Bongaerts, et al. 2018. Symbiodinium genomes reveal adaptive evolution of functions related to coral-dinoflagellate symbiosis. Commun Biol 1:95. https://doi.org/10.1038/s42003-018-0098-3.

Lobo, F. d. L., G. W. Nagel, D. A. Maciel, L. A. S. d. Carvalho, V. S. Martins, et al. 2021. AlgaeMAp: Algae Bloom Monitoring Application for Inland Waters in Latin America. Remote Sens 13:2874. https://doi.org/10.3390/rs13152874.

Margulis, L. 1971. Symbiosis and evolution. Sci Am 225:48-61. https://doi.org/10.1038/scientificamerican0871-48.

Martiny, J. B. H., S. E. Jones, J. T. Lennon, and A. C. Martiny. 2015. Microbiomes in light of traits: A phylogenetic perspective. Science 350:aac9323. https://doi.org/10.1126/science.aac9323.

Matthews, J. L., C. A. Oakley, A. Lutz, K. E. Hillyer, A. R. Grossman, V. M. Weis, and S. K. Davy. 2018. Partner switching and metabolic flux in a model cnidarian - Symbiodinium symbiosis. Proc R Soc B 285(1892). https://doi.org/10.1098/rspb.2018.2336.

McGill, B. J., B. J. Enquist, E. Weiher, and M. Westoby. 2006. Rebuilding community ecology from functional traits. Trends in Ecology and Evolution 21(4):178-185. https://doi.org/10.1016/j.tree.2006.02.002.

Miller, E. T., R. Svanbäck, and B. J. M. Bohannan. 2018. Microbiomes as Metacommunities: Understanding Host-Associated Microbes through Metacommunity Ecology. Trends in Ecology and Evolution 33(12):926-935. https://doi.org/https://doi.org/10.1016/j.tree.2018.09.002.

Morgenroth, T., and M. K. Ryan. 2021. The effects of gender trouble: An integrative theoretical framework of the perpetuation and disruption of the gender/sex binary. Perspectives on Psychological Science 16(6):1113-1142. https://doi.org/10.1177/1745691620902442.

Morris, J. J. 2018. What is the hologenome concept of evolution? Vers. 1. F1000Res 7:F1000. https://doi.org/10.12688%2Ff1000research.14385.1.

Nisbett, R. E., and T. Masuda. 2003. Culture and point of view. Proceedings of the National Academy of Sciences 100(19):11163-11170. https://doi.org/10.1073/pnas.1934527100.

Passoni, S., and C. Callieri. 2000. Picocyanobacteria single forms, aggregates and microcolonies: survival strategy or species succession? Int Vereinigung für Theor und Angew Limnol Verhandlungen 27:1879-1883. https://doi.org/10.1080/03680770.1998.11901567.

Pennisi, E. 2009. Origins. On the origin of cooperation. Science 325:1196-1199. https://doi.org/10.1126/science.325_1196.

Platt, A. J., and K. E. Whalen. 2023. Probing The Phycosphere: Techniques to Study Bacteria-Phytoplankton Interactions. Integrative and Comparative Biology; icad065. https://doi.org/10.1093/icb/icad065.

Raerinne, J. 2020. Ghosts of competition and predation past: Why ecologists value negative over positive interactions. Bulletin of the Ecological Society of America 101(4):e01766. https://doi.org/10.1002/bes2.1766.

Rapport, D. J. 1971. An optimization model of food selection. Am Nat 105:575-587. https://doi.org/10.1086/282746.

Reid, T., and J. Bergsveinson. 2021. How Do the Players Play? A Post-Genomic Analysis Paradigm to Understand Aquatic Ecosystem Processes. Front Mol Biosci 8:395. https://doi.org/10.3389/fmolb.2021.662888.

Schiebinger, L. 1991. The mind has no sex?: Women in the origins of modern science. Harvard University Press.

Seymour, J. R., S. A. Amin, J. B. Raina, and R. Stocker. 2017. Zooming in on the phycosphere: The ecological interface for phytoplankton-bacteria relationships. Nat Microbiol 2:17065. https://doi.org/10.1038/nmicrobiol.2017.65.

Shields, S. A., and S. Bhatia. 2009. Darwin on race, gender, and culture. Am Psychol 64:111. https://doi.org/10.1037/a0013502.

Simha, A., C. J. Pardo-De la Hoz, and L. N. Carley. 2022. Moving beyond the “diversity paradox”: the limitations of competition-based frameworks in understanding species diversity. Am Nat 200:89-100. https://doi.org/10.1086/720002.

Tilman, D. 1980. Resources: a graphical-mechanistic approach to competition and predation. Am Nat 116:362-393. https://doi.org/10.1086/283633.

Thompson, H. F., C. Lesaulnier, C. Pelikan, and T. Gutiérrez. 2018. Visualisation of the obligate hydrocarbonoclastic bacteria Polycyclovorans algicola and Algiphilus aromaticivorans in co-cultures with micro-algae by CARD-FISH. Journal of Microbiological Methods 152:73-79. https://doi.org/10.1016/j.mimet.2018.07.016.

Violle, C., M. Navas, D. Vile, E. Kazakou, C. Fortunel, et al. 2007. Let the concept of trait be functional! Oikos 116(5):882-892. https://doi.org/10.1111/j.0030-1299.2007.15559.x.

Wallenstein, M. D., and E. K. Hall 2012. A trait-based framework for predicting when and where microbial adaptation to climate change will affect ecosystem functioning. Biogeochemistry 109(1-3):35-47. https://doi.org/10.1007/s10533-011-9641-8.

West, S. A., A. S. Griffin, A. Gardner, and S. P. Diggle. 2006. Social evolution theory for microorganisms. Nat Rev Microbiol 4:597-607. https://doi.org/10.1038/nrmicro1461.

Wilson, W. G., and R. M. Nisbet. 1997. Cooperation and competition along smooth environmental gradients. Ecology 78(7):2004-2017. https://doi.org/10.1890/0012-9658(1997)078[2004:CACASE]2.0.CO;2.

From competition to cooperation: Paradigm shifts in trait-based ecology change our understanding of the processes that structure microbial communities

Downloads

Published

2023-11-15

How to Cite

Piccini, C., Devercelli, M., Yema, L., Segura, A., Bastidas Navarro, M., Sathicq, M. B., Martínez de la Escalera, G., Martínez Goicoechea, A., Rodrigues Amaral Da Costa, M., O’Farrell, I., Lara, E., & Kruk, C. (2023). From competition to cooperation: Paradigm shifts in trait-based ecology change our understanding of the processes that structure microbial communities. Ecología Austral, 33(3), 887–893. https://doi.org/10.25260/EA.23.33.3.0.2093