Mutualistic Symbioses


Mutualistic symbioses are defined as intimate inter‐species interactions beneficial to all species partners. In reality, however, mutualistic symbioses are more intricate, complex, diverse and variable than the formal definition suggests; understanding this complexity is essential to understanding mutualism dynamics. Widely distributed both geographically and taxonomically, mutualistic symbioses play a significant role in the biology of organisms. Iconic examples of mutualisms such as lichens, reef‐building corals with algal symbionts, and mycorrhizal fungi with terrestrial plants, highlight the prevalence of many symbiotic mutualisms in resource‐limited conditions. The several important examples of hereditary microbial symbiosis in insects call attention to the importance of hereditarily transmitted symbioses as well. But there are also mutualisms that do not fit the ecological paradigm of partnerships forged by nutrient scarcity, and evolutionarily persistent, horizontally‐transmitted mutualisms which challenge the notion that hereditary symbiosis is the only stable form of mutualistic symbiosis. In the face of ubiquitous immune defences among organisms, the persistence and ubiquity of mutualistic symbiosis seems a physiologically improbable phenomenon. But recent research suggests a possible resolution to this paradox, in revealing the involvement of immune mechanisms in selection, tolerance and maintenance of beneficial foreign microbes, as well as recognition and elimination of pathogens.

Key Concepts:

  • Given the ubiquity and effectiveness of immune defences among plants and animals, the existence of chronic, beneficial infections seems a physiologically improbable situation.

  • Despite its improbability, mutualistic symbiosis is widespread in the biosphere, playing key roles in the evolution and ecology of land plants, tropical and deep‐sea marine ecosystems, the biology of herbivorous animals, and more.

  • Mutualistic symbioses are diverse, embracing a physiologically, taxonomically, and ecologically diverse array of interactions.

  • Mutualistic symbioses can incorporate antagonistic as well as mutualistic elements; many can also vary in their biological effects, depending on environmental conditions.

  • While the metabolic foundation of many mutualistic host‐symbiont interactions lies in symbiotic‐enhanced nutrient exchanges in nutrient‐limited conditions, benefits of symbiotic mutualisms can also include nonnutritional factors such as bioluminescence, drought resistance and enhanced defences against predators and pathogens.

  • Hereditarily‐transmitted symbioses are often considered the 'ultimate' mutualisms because of the extreme interdependence and striking coevolution of hosts and endosymbionts in such interactions.

  • However, nonhereditary (horizontally transmitted) mutualisms also can be strongly interdependent, evolutionarily persistent associations, with major impact on the ecology and evolution of plants and animals.

Keywords: symbiosis; mutualism; parasite; lichens; legumes; symbiont; host; endosymbiont; bioluminescence; mycorrhizae; reef‐building corals; endophytes


Beiler JK, Durall DM, Simard SW, Maxwell SA and Kretzer AM (2009) Architecture of the wood‐wide web: Rhizopogon spp. genets link multiple Douglas‐fir cohorts. New Phytologist 185: 543–553.

Bonfante P and Selosse M‐A (2010) A glimpse into the past of land plants and of their mycorrhizal affairs: from fossils to evo‐devo. New Phytologist 186: 267–270.

Bordenstein SR, Paraskevopoulos C, Dunning Hotopp JC et al. (2009) Parasitism and mutualism in Wolbachia: what the phylogenomic trees can and cannot say. Molecular Biology and Evolution 26: 231–241.

Boucher D (1982) The ecology of mutualism. Annual Review of Ecology and Systematics 13: 315–347.

Breznak J and Brune A (1994) Role of microorganisms in the digestion of lignocellulose by termites. Annual Review of Entomology 39: 453–487.

Cerf‐Bensussan N and Gaboriau‐Routhiau V (2010) The immune system and the gut microbiota: friends or foes? Nature Reviews Immunology 10: 735–744.

Dethlefsen L, Mcfall‐Ngai MJ and Relman DA (2007) An ecological and evolutionary perspective on human–microbe mutualism and disease. Nature 449: 811–818.

Distel DL, Amin M, Burgoyne A et al. (2011) Molecular phylogeny of Pholadoidea Lamarck, 1809, supports a single origin for xylotrophy (wood feeding) and xylotrophic bacterial endosymbiosis in Bivalvia. Molecular Phylogenetics and Evolution 61: 245–254.

Dubilier N, Bergin C and Lott C (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nature Reviews Microbiology 6: 725–740.

Finlay RD (2008) Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. Journal of Experimental Botany 59: 1115–1126.

Goffredi SK, Orphan VJ, Rouse GW et al. (2005) Evolutionary innovation: a bone‐eating marine symbiosis. Environmental Microbiology 7: 1369–1378.

Hansen AK and Moran NA (2014) The impact of microbial symbiots on host plant utilization by herbivorous insects. Molecular Ecology 23: 1473–1496.

Heddi A, Lefebrvre F and Nardon P (1993) Effect of endocytobiotic bacteria on mitochondrial enzymatic activities in the weevil Sitophilus oryzae (Coleoptera: Cucculionidae). Insect Biochemistry and Molecular Biology 23: 403–411.

Hibbett DS, Gilbert L‐B and Donoghue MJ (2000) Evolutionary instability of ectomycorrhizal symbioses in basidiomycetes. Nature 407: 506–508.

Hoeksema JD, Chaudhary VB, Gehring CA et al. (2010) A meta‐analysis of context‐dependency in plant response to inoculation with mycorrhizal fungi. Ecology Letters 13: 394–407.

Hungate RE (1975) The rumen microbial ecosystem. Annual Review of Ecology and Systematics 6: 39–66.

Husnik F, Nikoh N, Koga R et al. (2013) Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 153: 1567–1578.

Husseneder C (2010) Symbiosis in subterranean termites: a review of insights from molecular studies. Environmental Entomology 39: 378–388.

Jones MD and Smith SE (2004) Exploring functional definitions of mycorrhizas: are mycorrhizas always mutualisms? Canadian Journal of Botany 82: 1089–1109.

Jones JDG and Dangl JL (2006) The plant immune system. Nature 444: 323–329

Karasov WH and Carey HV (2009) Metabolic teamwork between gut microbes and hosts. Microbe 323–328.

Kiers ET, Denison RF, Kawakita A and Herre EA (2011) The biological reality of host sanctions and partner fidelity. Proceedings of the National Academy of Sciences of the USA 108: E7.

Kiers ET and van der Heijden MGA (2006) Mutualistic stability in the arbuscular mycorrhizal symbiosis: exploring hypotheses of evolutionary cooperation. Ecology 87: 1627–1636.

Kim M, Morrison M and Yu Z (2011) Status of the phylogenetic diversity census of ruminal microbiomes. FEMS Microbiology Ecology 76: 49–63.

Knowlton N and Rohwer F (2003) Multispecies microbial mutualisms on coral reefs: the host as a habitat. American Naturalist 162(suppl.): s51–s62.

Krause DO, Nagaraja TG, Wright ADG and Calloway TR (2013) Board‐invited review: Rumen microbiology: leading the way in microbial ecology. Journal of Animal Science 91: 331–341.

Lackner G, Moebius N, Partida‐Martinez LP, Boland S and Hertweck C (2011) Evolution of an endofungal lifestyle: deductions from the Burkolderia rhizoxinica genome. BMC Genomics 12: 210

Ley RE, Lozupone CA, Hamady M, Knight R and Gordon JI (2008) Worlds within worlds: evolution of the vertebrate gut microbiota. Nature Reviews Microbiology 6: 776–788.

Lutzoni F and Miadlikowska J (2009) Lichens. Current Biology 19: R502–R503.

Margulis L (1993) Symbiosis in Cell Evolution, 2nd edn. San Francisco, CA: WH Freeman.

Mcfall‐Ngai MJ (2007) Adaptive immunity: care for the community. Nature 445: 153.

Mcfall‐Ngai MJ, Hadfield MG, Bosch TCG et al. (2013) Animals in a bacterial world, a new imperative for the life sciences. Proceedings of the National Academy of Sciences of the USA 110: 3229–3236.

Moran NA, McCutcheon JP and Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annual Review of Genetics 42: 165–190.

Müller WEG and Müller IM (2003) Metazoan immune system: identification of the molecules and their functions in sponges. Integrative and Comparative Biology 43: 281–292.

Nelson MC and Graf J (2012) Bacterial symbioses of the medicinal leech Hirudo verbena. Gut Microbes 3: 322–331.

Nyholm SV and Graf J (2012) Knowing your friends: invertebrate innate immunity fosters beneficial bacterial symbioses. Nature Reviews Microbiology 10: 815–827.

Nyholm SV and McFall-Ngai MJ (2004) The winnowing: establishing the squid-Vibrio symbiosis. Nature Reviews Microbiology 2: 632–642.

Oliver KM, Degnan PH, Burke GR and Moran N (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annual Review of Entomology 55: 247–266.

Owen J, Punt J and Stranford S (2012) Kuby Immunology, 7th edn, p. 571. New York: WH Freeman.

Pringle A and Bever JD (2008) Analogous effects of arbuscular mycorrhizal fungi in the laboratory and a North Carolina field. New Phytologist 180: 162–175.

Randow F, MackMicking JD and James LC (2013) Cellular self‐defense: how cell‐autonomous immunity protects against pathogens. Science 340: 701–706.

Rikkinen J and Poinar GO (2008) A new species of Phyllopsora (Lecanorales, lichen‐forming Ascomycota) from Dominican amber, with remarks on the fossil history of lichens. Journal of Experimental Botany 59: 1007–1011.

Rodriguez R and Redman R (2008) More than 400 million years and plants still can't make it on their own: plant stress tolerance via fungal symbiosis. Journal of Experimental Botany 59: 1109–1114.

Rodriguez RJ, White JF, Arnold AE and Redman RS (2009) Fungal endophytes: diversity and functional roles. Tansley Review, New Phytologist 182: 314–330.

Ronald PC and Beutler B (2010) Plant and animal sensors of conserved microbial signatures. Science 330: 1061–1064.

Rooks MG and Garrett W (2011) Bacteria, food and cancer. F1000 Biology Reports 3: 12. doi: 10.3410/B3‐12.

Sachs JL, Essenberg CJ and Turcotte MM (2011) New paradigms for the evolution of beneficial infections. Trends in Ecology and Evolution 26: 202–209.

Sachs JL and Simms EL (2006) Pathways to mutualism breakdown (2006) Trends in Ecology and Evolution 21: 585–592.

Saffo MB (1991) Symbiosis in evolution. In: Dudley EC (ed.) The Unity of Evolutionary Biology, pp. 674–680. Portland, OR: Dioscorides Press.

Saffo MB (1993) Coming to terms with a field: words and concepts in symbiosis. Symbiosis 14: 17–31.

Saffo MB (2001) Complexity, variability and change in symbiotic associations. Family Systems 6: 3–18.

Saffo MB, McCoy AM, Rieken C and Slamovits CH (2010) Nephromyces, a beneficial apicomplexan symbiont in marine animals. Proceedings of the National Academy of Sciences of the USA 107: 16190–16195.

Sanders WB (2006) A feeling for the superorganism: expression of plant form in the lichen thallus. Botanical Journal of the Linnaean Society 150: 89–99.

Sekirov I, Russell SL, Caetano L, Antunes M and Finlay BB (2010) Gut microbiota in health and disease. Physiological Reviews 90: 859–904.

Selosse M‐A, Baudoin E and Vandenkoornhuyse P (2004) Symbiotic microorganisms, a key for ecological success and protection of plants. Comptes Rendus Biologie 327: 639–648.

Selosse M‐A, Richard F, He X and Simard SW (2006) Mycorrhizal networks: des liaisons dangereuses? Trends in Ecology and Evolution 21: 621–628.

Shigenobu S and Wilson ACC (2011) Genomic revelations of a mutualism: the pea aphid and its obligate bacterial symbiont. Cellular and Molecular Life Sciences 68: 1297–1309.

Silver AC, Kikuchi Y, Fadl AA et al. (2007) Interaction between innate immune cells and a bacterial III system in mutualistic and pathogenic associations. Proceedings of the National Academy of Sciences of the USA 104: 9481–9486.

Soto MJ, Domínguez‐Ferreras A, Pérez‐Mendoza D, Sanjuan J and Olivares J (2009) Mutualism versus pathogenesis: the give‐and‐take in plant‐bacteria interactions. Cellular Microbiology 11: 381–388.

Sprent J (2007) Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytologist 174: 11–25.

Suen G and Currie C (2008) Ancient fungal farmers of the insect world. Microbiology Today 35: 172–175.

Tedersoo L and Nara K (2010) General latitudinal gradient of biodiversity is reversed in ectomycorrhizal fungi. New Phytologist 185: 351–354.

U'Ren JM, Lutzoni F, Miadlikowska J, Laetsch AD and Arnold AE (2012) Host and geographic structure of endophytic and endolichenic fungi at a continental scale. American Journal of Botany 99: 898–914.

Venn AA, Loram JE and Douglas AE (2008) Photosynthetic symbioses in animals. Journal of Experimental Botany 59: 1069–1080.

Vitousek P, Cassman K, Cleveland C et al. (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57/58: 1–45.

Wang B, Yeun LH, Xue J‐Y et al. (2010) Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants. New Phytologist 186: 514–525.

Wernegreen JJ (2005) For better or worse: genomic consequences of intracellular mutualism and parasitism. Current Opinion in Genetics and Development 15: 572–583.

Wernegreen JJ and Wheeler DE (2009) Remaining flexible in old alliances: functional plasticity in constrained mutualisms. DNA and Cell Biology 28: 371–381.

Weyl EG, Frederickson ME, Yu DW and Pierce NE (2010) Economic contract theory tests models of mutualism. Proceedings of the National Academy of Sciences of the USA 107: 15712–15716.

Weyl EG, Frederickson ME, Yu DW and Pierce NE (2011) Reply to Kiers et al.: economic and biological clarity in the theory of mutualism. Proceedings of the National Academy of Sciences of the USA 108: E8.

Yellowlees D, Rees TAV and Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant, Cell and Environment 31: 679–694.

Zahran HH (1999) Rhizobium‐legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiology and Molecular Biology Reviews 63: 968.

Further Reading

Douglas AE (2010) The Symbiotic Habit. Princeton, NJ: Princeton University Press.

Hibbett DS (2002) When good relationships go bad. Nature 419: 345–346.

Knowlton N (2008) Coral reefs. Current Biology 18: R18–R21.

Margulis L and Fester R (eds) (1991) Symbiosis as a Source of Evolutionary Innovation. Cambridge, MA: MIT Press.

McFall‐Ngai MJ (2008) Hawaiian bobtail squid. Current Biology 18: R1043–R1044.

Mukhopadhyay R (2007) How shipworms get their nitrogen fix. Analytical Chemistry 79: 8831.

Pringle A (2009) Mycorrhizal networks. Current Biology 19: R838–R839.

Russell J, Dubilier N and Rudgers J (2014) Nature's microbiome: introduction. Molecular Ecology 23: 1225–1237.

Smith DC and Douglas AE (1987) The Biology of Symbiosis. London, UK: Edward Arnold.

Smith SE and Read D (2008) Mycorrhizal Symbiosis, 3rd edn. Amsterdam: Elsevier.

Wernegreen J (2012) Endosymbiosis. Current Biology 22: R555–R561.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Saffo, Mary Beth(Jul 2014) Mutualistic Symbioses. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1002/9780470015902.a0003281.pub2]