Mutualistic Symbioses

Mutualistic Symbioses Introductory article Mary Beth Saffo, National Science Foundation, Arlington, Virginia, USA Article Contents . The Improbability of Beneficial Symbiotic Associations This article was based on work supported by the U.S. National Science Foundation (NSF), while working for the NSF. Any opinion or perspective expressed in this article is that of the author and does not necessarily reflect the views of the NSF. . Defining Mutualistic Symbiosis . The Distribution of Mutualistic Symbioses . Do Immune Defenses Keep Mutualisms Together? The Importance of Partner Choice Online posting date: 15th July 2014 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, reefbuilding 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. The Improbability of Beneficial Symbiotic Associations ‘Know thyself’ is not just a philosophical maxim, but a basic requirement of life itself. The product of philosophical selfeLS subject area: Ecology How to cite: Saffo, Mary Beth (July 2014) Mutualistic Symbioses. In: eLS. John Wiley & Sons, Ltd: Chichester. DOI: 10.1002/9780470015902.a0003281.pub2 knowledge is (hopefully) thoughtful, useful human beings; the product of biological self-knowledge is protection of the structural and genomic integrity of each organism. A key challenge for life is preservation of this integrity in a way that still allows the controlled interaction with the environment on which life also depends. Central to preservation of organismal integrity are mechanisms for recognition of ‘self’ and ‘non-self’, and defensive mechanisms for protection of self against nonself. Many molecular and structural features of organisms are involved in both of these functions of self/non-self recognition and self-protection. For instance, physical boundaries of organisms – cell membranes, cell walls, epidermal and extra-epidermal barriers – simultaneously define and protect an organism’s ‘self’. Similarly, several molecular mechanisms for self/non-self recognition are also integral components of the various immune defences that protect organisms against invasion by foreign organisms and foreign genomes (Ronald and Beutler, 2010; Owen et al., 2012; Randow et al., 2013). See also: Immune System; Innate Immune Mechanisms: Nonself Recognition; Plant Defences against Herbivore Attack Although vertebrate immune systems are the best characterised, invertebrate animals and plants also have impressive immune mechanisms (Jones and Dangl, 2006; Owen et al., 2012; Randow et al., 2013). Even animals as ‘lowly’ as sponges, for instance, possess exquisitely sensitive abilities for recognition and rejection of non-self genotypes, with molecular mechanisms bearing at least some resemblance to graft-rejection processes in humans (Müller and Müller, 2003). See also: Immune Defence: Microbial Interference; Immunology of Invertebrates: Humoral; Plant Innate Immunity; Porifera (Sponges) Given the undesirable, and sometimes dire, effects of parasites and pathogens that breach immune defences of their plant or animal hosts, and the serious consequences of immune system malfunction for those hosts, it is not surprising that physicians, veterinarians and plant pathologists have long considered elimination of infection as a central goal of medical and agricultural practice. Until the 1970s, ecologists also thought of species interactions in largely antagonistic terms, viewing unfriendly inter-species encounters such as predator–prey interactions, competition and infectious diseases as the key biotic factors shaping biological communities. Mutually beneficial interactions, however, were considered to be rare This is a US Government work and is in the public domain in the United States of America. eLS & 2014, John Wiley & Sons, Ltd. www.els.net 1 Mutualistic Symbioses and ecologically unimportant, a view reinforced by early mathematical models that concluded that mutualism was an unstable – literally, an inconceivable – class of species interaction (for history, see Boucher, 1982). Today, mutualisms are the subject of serious scientific attention by ecologists, evolutionary biologists, physiologists and molecular biologists. We know that mutualistic symbioses are widespread in the biosphere; there is strong evidence that many of these interactions have had, and continue to have, important effects on the evolution and ecology of organisms (Mcfall-Ngai et al., 2013). There is also a growing awareness in both medicine and agriculture that certain microbial infections can enhance, and, in some cases, may be essential to, plant and animal (including human) health (Dethlefsen et al., 2007; Ley et al., 2008; Pringle and Bever, 2008; Rooks and Garrett, 2011; Sekirov et al., 2010). See also: Endosymbionts; Plant–Fungal Interactions in Mycorrhizas; Plastid Origin and Evolution Nevertheless, there is still much to learn about the physiological and evolutionary dynamics of mutualistic symbiotic associations. Whatever the unique features of the symbiotic association that is their focus, researchers of symbiotic mutualisms find themselves asking similar questions. Can plant and animal hosts distinguish between harmful microbes and the ‘good guys’, and, if so, how do they make that distinction? What factors make microbial infection ‘good’ for its hosts? How, indeed, does one determine whether a symbiotic interaction is ‘good’ for hosts or symbionts? What kinds of metabolites are transported between partners, and which ones are the key metabolic currencies in the symbiotic interaction? Are mutualistic interactions equal partnerships, or does one symbiotic partner still have more influence or ‘control’ over the association than the other? Are there certain ecological conditions that favour mutualistic symbioses? What are the selection pressures that favour mutualistic interactions? How are these associations maintained generation after generation, and how do the associations shape the evolution of both hosts and symbionts? Above all, there remains the question of the improbability of mutualistic symbiosis: how and why do beneficial infections persist in the face of pervasive, powerful defences against ‘non-self’? Defining Mutualistic Symbiosis In theory, mutualistic symbiosis is a simple-to-understand phenomenon: a symbiotic association that is beneficial to both (or all) symbiotic partners. In reality, however, mutualistic symbioses are more complex, more diverse and less well-understood than their simple definition suggests (Saffo, 1993). Rather than merely cluttering our understanding with confusing detail, this diversity and complexity reveals much about the real-life dynamics of mutualistic interactions. One kind of complication arises from the fact that even the most well-known mutualisms are still not fully understood. Often, we understand more about the effects of the 2 symbiosis on the hosts than on the microbial symbionts. In reef-building corals, for instance, the benefits of symbiosis to one partner (the coral hosts) have been demonstrated clearly, while the effects of symbiosis on the other species partner (Symbiodinium, dinoflagellates residing within the gastrodermal cells of corals) are unknown or a matter of debate (Knowlton and Rohwer, 2003; Yellowlees et al., 2008). The benefits (or not) of symbiosis to the photobionts (algal symbionts) of lichens or to the nitrogen-fixing bacteria (rhizobia) inhabiting root nodules of legumes are similar perennial questions (Sanders, 2006; Sachs and Simms, 2006; Venn et al., 2008; Lutzoni and Miadlikowska, 2009). See also: Algal Symbioses; Dinoflagellates; Green Algae; Lichens; Root Nodules (Legume–Rhizobium Symbiosis) In other, less-studied, but seemingly benign symbioses, benefits to symbionts and hosts have been hypothesised, but have received little direct investigation. Complicating the problem of elucidating those benefits is the fact that ‘benefit’ can be a tricky parameter to assay. Short-term, laboratory-based experiments can be a misleading indicator of long-term evolutionary outcome in nature, even more so in a strongly integrated symbiosis where one species partner cannot be separated easily from the other (but see Pringle and Bever, 2008). For many symbiotic interactions, ‘benefit’ is necessarily inferred, rather than measured directly. For instance, unlike parasitisms (where symbiont prevalence can vary in space and time across a host species, but is always less than 100%), many obligately symbiotic microbes regularly have a prevalence of 100% throughout populations of a single host species, sometimes even throughout entire clades (Moran et al., 2008; Bonfante and Selosse, 2010; Saffo, 1991; Saffo et al., 2010; Wang et al., 2010), a physiologically and ecologically surprising statistic strongly suggestive of mutual benefit or mutual need. In some cases, benefit is inferred from the synergistic effects of the symbiotic partnerships. In lichens, for example (Table 1), many chemicals produced by the lichen symbiosis are not produced by either the algal or fungal partner alone, but only by the symbiotic partnership; the morphologies of lichens transcend the mere sum of their algal and fungal parts (Sanders, 2006); and lichens famously thrive in sometimes-extreme habitats where especially the fungal partners cannot survive alone (Lutzoni and Miadlikowska, 2009). See also: Algal Symbioses; Ascomycota; Lichens Benefit can also be inferred from demonstration of physiological or reproductive dependence of the hosts and symbionts on the symbiotic association (Bordenstein et al., 2009; Husseneder, 2010; Moran et al., 2008; Selosse et al., 2004). For organisms that cannot survive without their symbiotic species partners, maintenance of that symbiosis is without question beneficial to those organisms, at least in terms of physiological necessity. (The long-term evolutionary consequences of such extreme dependence is another perennial topic of evolutionary debate, though some clades of highly interdependent symbioses have shown impressive evolutionary persistence: Moran et al. This is a US Government work and is in the public domain in the United States of America. eLS & 2014, John Wiley & Sons, Ltd. www.els.net Mutualistic Symbioses Table 1 Some examples of mutualistic symbiosis Hosts Symbionts Distribution References Reef-building corals Symbiodinium, photosynthetic dinoflagellates Chlorella Tropical oceans Venn et al. (2008), Yellowlees et al. (2008) Fresh water Chemolithoautorophs (sulphur-oxidizing bacteria; also methanogens in some animals) Arbuscular mycorrhizal fungi (Glomeromycota); Ectomycorrhizal fungi (mostly basidiomycetes) and ericoid mycorrhizae (ascomycetes and basidiomycetes) Fungal endophytes Sulfide-rich marine waters Venn et al. (2008), Yellowlees et al. (2008) Dubilier et al. (2008) Chlorohydra Vestimentiferan annelid worms, lucinid clams and several other invertebrates Land plants (85% of vascular plant families) Most vascular plants Lichens: mycobionts (mostly ascomycetes) Legumes (Fabaceae) Pomocentrid fish and Bobtail squid (Euprymna) Termites Lichen photobionts (mostly green algae; some cyanobacteria) Rhizobium in legume roots Bacteria: Vibrio fischeri Bacteria and protists in termite mid-gut Bacteria in gills Shipworms (wood-boring clams) Herbivorous vertebrates Bacteria and protists in rumen Bacteria Aphids Leeches Ralstonia (fungal pathogen of plants) Molgulid tunicates Cockroaches Filarial nematodes and some insects Leaf-cutting ants Bacteria Bacteria Terrestrial environments, especially nutrient-poor soils Selosse et al. (2006), Finlay (2008), Bonfante and Selosse (2010) Terrestrial environments, especially nutrient-poor soils Exposed terrestrial or intertidal habitats U’Ren et al. (2012), Rodriguez et al. (2009) Lutzoni and Miadlikowska (2009) Terrestrial soils Shallow and middle-depth ocean waters Terrestrial: wood Sachs and Simms (2006), Sprent (2007) Nyholm and McFall-Ngai (2004) Husseneder (2010) Marine: wood Distel et al. (2011) Mostly terrestrial Karasov and Carey (2009), Ley et al. (2008) Moran et al. (2008), Shigenobu and Wilson (2011) Nelson and Graf (2012) Lackner et al. (2011) Terrestrial plants (phloem feeders) Terrestrial plant roots Apicomplexan protest (Nephromyces) and bacteria within Nephromyces Bacteria in gut and fat body Temperate-high latitude and marine benthic habitats Saffo et al. (2010) Terrestrial Wolbachia Terrestrial Bacteria: urate catabolism (among other activities) Bordenstein et al. (2009) Fungi (Escovopsis) Terrestrial Suen and Currie (2008) (2008).) See also: Endosymbionts; Natural Selection: Introduction Even in those symbioses in which all species partners are known to benefit from their symbiotic association with each other, the dynamics of such interactions can still be intricate, complex, difficult to assay and resistant to easy characterisation (Moran et al., 2008). In newly described symbioses, even state-of-the-art genomic, transcriptomic or metabolic data alone cannot necessarily resolve the key benefits (or dependencies) of a symbiotic mutualism, especially if the organismal, ecological or evolutionary context is not given consideration, or if that context is still poorly understood (e.g. Bordenstein et al., 2009). Full understanding of the integrated relationships of symbiotic associations demands an equally integrative perspective on part of the scientists who study them. This is a US Government work and is in the public domain in the United States of America. eLS & 2014, John Wiley & Sons, Ltd. www.els.net 3 Mutualistic Symbioses The issue of ‘benefit’ is further complicated by the fact that the beneficial effects of symbiotic interactions are often enmeshed in various ways with harmful ones. Data on wellstudied symbioses, such as arbuscular mycorrhizae or algal-infected ‘green hydra’, have shown that there can be a significant cost to mutualistic symbiosis, no matter how important its benefits are. The balance between cost and benefit to partners of such symbioses can vary with environmental conditions; in certain situations, when costs outweigh benefits, some mutualistic symbioses veer into parasitism, or fail to form, or fall apart. (Bordenstein et al., 2009; Finlay, 2008; Hoeksema et al., 2010; Jones and Smith, 2004; Sachs and Simms, 2006; Sachs et al., 2011; Saffo, 1993, 2001; Selosse et al., 2006; Silver et al., 2007). Environmental factors capable of shifting interaction dynamics in this way can include not only physical parameters such as nutrient availability, temperature or light, but also biotic features such as the particular species or strain of symbiotic partner, the introduction of additional symbiotic partners or the presence of non-symbiotic interacting species, such as predators, competitors or nonsymbiotic mutualists. For instance, some bacteria and fungi can operate as pathogens or mutualists, depending on the species of their plant or animal host that they infect, or (as in several mycorrhizal fungi), levels of phosphorus in the soil (Jones and Smith, 2004; Silver et al., 2007). Finally, in symbioses involving three or more interacting species partners, antagonistic interactions can co-occur with beneficial ones. In some cases, enhancement of antagonistic interactions is even the key benefit provided by mutualistic endosymbionts, through endosymbiont production of antibiotics or toxins, enhancement of host immune or antipredation defenses or enhancement of host pathogenicity (e.g. Table 1; Lackner et al., 2011). See also: Interspecific Interaction; Mutualism Among Free-living Species; Parasitism: The Variety of Parasites Genomic data suggest that interaction outcomes of some microbial symbioses can be evolutionarily malleable as well. Several mutualistic microbes show close phylogenetic relationships to microbial pathogens; mutualistic and antagonistic microbes also share a number of homologous mechanisms for infection and colonisation of their hosts (Moran et al., 2008; Saffo et al., 2010; Silver et al., 2007; Wernegreen, 2005). Yet another complication is the fact that mutualistic symbioses are not uniform; they differ in degrees of host– symbiont dependency, in magnitude and kinds of benefits, in numbers and kinds of symbiotic partners, in location of symbionts within their hosts, in geographical distribution and ecological context, in modes of symbiont-to-host transmission, in species specificity of host–symbiont partnerships, in their evolutionary history and in variability of host–symbiont dynamics over space and time. All of these factors affect the nature of host–symbiont interactions. There is, in short, no single, optimal formula for a ‘perfect’ beneficial symbiosis. Margulis (1993) once defined symbiosis as a ‘parasexual phenomenon’ – a kind of interspecies ‘marriage’, in which 4 the lives of two or more species are intertwined, in protracted intimate association – or, in the case of mutualistic symbiosis, one of the overall mutual benefits to the species partners in question. Like marriages, mutualistic symbioses can be complex: they have costs as well as benefits; the diversity and intricacy of their multiple interactions and interdependencies often defy easy analysis; and their internal dynamic can be influenced – sometimes profoundly – by external conditions (Saffo, 2001). See also: Margulis, Lynn; Mutualism Among Free-living Species The Distribution of Mutualistic Symbioses Mutualistic symbioses are everywhere. Geographically, they are widely distributed, occurring throughout terrestrial and aquatic ecosystems, at all ocean depths, at all altitudes and all latitudes. Taxonomically, they are also widely distributed: species partners include representatives of animals, plants, fungi, protists, eubacteria and archaea (see Table 1 for some examples of such partnerships). Moreover, the list of such partnerships continues to grow in number and in diversity: increasing interest in mutualism and symbiosis among biologists, coupled with advances in genomics and other investigative methods, continues to uncover new examples of mutually beneficial symbiosies. Within the last 30 or 40 years, whole new classes of mutualistic symbioses have been discovered, such as symbioses between wood-boring clams and bacteria (Distel et al., 2011), and between chemoautotrophic bacteria and marine invertebrate animals (Dubilier et al., 2008). Others, such as symbioses between marine animals and bioluminescent bacteria (Nyholm and McFall-Ngai, 2004), hereditary bacterial symbioses of insects (Moran et al., 2008; Husnik et al., 2013; Hansen and Moran, 2014) or plant symbioses with fungal endophytes (Rodriguez et al., 2009; U’Ren et al., 2012) have grown from interesting natural history anecdotes into systems of experimental and/or ecological importance which have generally enlarged our understanding of symbiosis. Though a widespread and evolutionarily consequential endosymbiont of insects, nematodes and some terrestrial crustaceans, the bacterium Wolbachia has rarely been considered an unequivocally beneficial presence for its host; but recent work has shown nevertheless that in a few hosts – filarial nematodes and at least one insect species –Wolbachia can be a mutualist (Bordenstein et al., 2009). Still other symbioses have been found in unexpected places, or have been found to have unexpected ecological and physiological dimensions (Lackner et al., 2011; Saffo et al., 2010). Even in the last decade, surprising new mutualisms have been found: one particularly astonishing example is the recent discovery of deep-sea polychaete annelids that make their living exclusively on submerged mammalian skeletons, with the help of heterotrophic lipid-metabolizing bacterial endosymbionts (Goffredi et al., 2005; Dubilier et al., 2008). See also: This is a US Government work and is in the public domain in the United States of America. eLS & 2014, John Wiley & Sons, Ltd. www.els.net Mutualistic Symbioses Bioluminescence; Diversity of Life; Hydrothermal Vent Communities; Microevolution and Macroevolution: Introduction From all this diversity, can we glean patterns that might illuminate the factors that foster and maintain mutualistic associations? While some general principles can be distilled from consideration of selected mutualisms, few generalisations apply to all mutualistic interactions. The exceptions to those generalisations are worth careful attention, as they expand our understanding of the phenomenon and provoke fresh questions about their mechanics and biological significance of mutualistic associations. GENERALISATION 1. Mutualistic symbiosis is prevalent in nutrient-limited habitats, and in animals with nutrient-limited diets. The nutritional contributions of each partner tend to complement, rather than duplicate, those of the other. Many of the best-studied mutualisms involve provision or transport of organic and/or inorganic nutrients between hosts and symbionts; and these are indeed most prevalent in nutrient-limited conditions. In such nutritionally-based mutualisms, the metabolic contributions of hosts and symbionts tend to complement each other: heterotrophs partner with autotrophs, and plants or animals partner with microbes which possess metabolic capabilities absent from their hosts. In heterotroph–autotroph symbioses, the heterotrophic partner (fungi or invertebrate animals) provides inorganic nutrients (nitrogen, phosphorus, sulphur, carbon dioxide or oxygen) to its autotrophic symbionts (plants, algae, photosynthetic or chemosynthetic bacteria), while the autotrophic partner supplies organic carbon to its heterotrophic host (Venn et al., 2008; Yellowlees et al., 2008). In adult animals that lack mouths – such as gutless marine oligochaete or polychaete worms with chemoautrotrophic bacterial symbionts- or those that do not feed as adults – such as the marine flatworm Symsagittifera (formerly Convoluta) roscoffensis, with green algal symbionts – it is particularly obvious that hosts must be strongly dependent on their autotrophic hosts for provision of fundamental nutrients. See also: Green Algae; Hydrothermal Vent Communities; Platyhelminthes (Flatworms) Similarly, herbivorous animals, or other animals making their living on difficult-to-digest and/or nutritionally limited diets such as blood, phloem, wood, plant leaves (ruminants, aphids, leeches, termites, among many other examples) rely on symbionts to provide the vitamins, amino acids or other nutrients absent in the host’s food, and/or enzymes necessary to digest that food (Distel et al., 2011; Husseneder, 2010; Karasov and Carey, 2009; Ley et al., 2008; Moran et al., 2008; Shigenobu and Wilson, 2011). One measure of the impact of such symbionts is the sheer number and biomass of gut symbionts in some animals. In termites, for instance, gut bacteria and protozoa account for  30% of termite biomass (Breznak and Brune, 1994); similarly, an individual grain weevil (Sitophilus oryzae) contains 1–3 million intracellular bacteria, approximately equal to the number of host weevil cells (Heddi et al., 1993). The rumen of cows and other ruminant mammals contains a diverse and dense microflora, comprising approximately 104 species of prokaryotes (both eubacteria and archaea) and at least 23 species of eukaryotic microbes, in concentrations of 1010 –1011 prokaryotic cells and  106 eukaryotic (protistan and fungal) cells per millilitre; a single 50–100 L rumen of a large adult ruminant thus harbours a staggering number of microbes: 500– 1000 trillion bacterial cells and 50–100 billion protozoa per animal (Hungate, 1975; Kim et al., 2011; Krause et al., 2013). See also: Animal Nutrient Requirements; Cellulose: Biogenesis and Biodegradation; Ecology of Invertebrate Nutrition; Rumen; Vertebrate Herbivory and Its Ecosystem Consequences Symbiotic nitrogen-fixing bacteria (rhizobia, actinorrhizal bacteria and some cyanobacteria) provide metabolically-useable nitrogen to plants in nitrogen-poor soils (legumes, alders and other plants) and animals (some termites and several marine invertebrates) in nitrogenlimited environments (Table 1). Symbiotic nitrogen fixation is a significant component of biological nitrogen fixation worldwide, and may even equal or exceed rates of nitrogen fixation by free-living bacteria in oceans and terrestrial soils. Among cultivated legumes alone, yearly levels of nitrogen fixation have been estimated at more than 40 t per year, about half the yearly global industrial production of nitrogen fertilizer. (Zahran, 1999; Vitousek et al., 2002). See also: Agricultural Production; Coevolution: plant– Microorganism; Nitrogen Fixation; Rhizobium and Other N-fixing Symbioses; Root Nodules (Legume–Rhizobium Symbiosis) Terrestrial plant roots are characteristically associated with a number of microbial symbionts, especially in soils low in nitrogen and phosphorus (Selosse et al., 2004; Sprent, 2007). In addition to the association of some plant roots with nitrogen-fixing bacteria (see above), the roots of all but a few vascular plant families form mycorrhizae (‘fungus roots’) with various fungal taxa. Root-associated fungi plant their ‘feet’ (or, more accurately, their hyphae) in two worlds: in intimate connections with plant tissues at one end, and also in surrounding soil. From the physical arrangement alone, while also coupled crucially with biochemical capabilities which make these activities possible, it is easy to see how mycorrhizal fungi can enhance uptake and transport of nitrogenous compounds and phosphate from soil to plant roots (Finlay, 2008). In return, fungi acquire organic carbon through the photosynthetic activities of their host plants. Among the major variants of mycorrhizal fungi, arbuscular mycorrhizal fungi (in the Glomeromycota) are obligate symbionts which penetrate root cells; infecting the majority of terrestrial plants, they are very widely distributed among plants from all latitudes, including not only angiosperms, but also mosses, ferns and gymnosperms. Ectomycorrhizal fungi, mostly basidiomycetes or ascomycetes, penetrate plant roots, but do not penetrate plant cell walls; they are characteristic colonists of trees such as oaks, beeches, eucalypts and many This is a US Government work and is in the public domain in the United States of America. eLS & 2014, John Wiley & Sons, Ltd. www.els.net 5 Mutualistic Symbioses gymnosperms. These associations may have impact beyond the effects on single trees; recent work suggests that, at least in Douglas fir, ectomycorrhizae can connect simultaneously to more than one tree, a phenomenon with provocative ecological implications (Beiler et al., 2009); in associating simultaneously with non-photosynthetic and photosynthetic plants, certain ectomycorrhizae can also serve as physiological links between these plants, siphoning nutrients from photosynthetic plants to non-photosynthetic plant parasites. See also: Ascomycota; Basidiomycota; Mycorrhiza; Plant–Fungal Interactions in Mycorrhizas; Roots: Contribution to the Rhizosphere; Roots and Root Systems Several aquatic invertebrate animals are also partners in autotroph–heterotroph associations of ecological importance. Corals, especially those in shallowest waters, are highly dependent on their dinoflagellate symbionts, whose photosynthetic products supply up to 90% of the organic carbon needs of their hosts; dinoflagellate symbiosis also enhances the growth of the hard, calcareous skeletons of corals, on which coral health, and the physical architecture of the reef ecosystem, depends. The dependence of corals on dinoflagellate symbionts is further reflected in the devastating effect of ‘coral bleaching’ – the expulsion of dinoflagellate symbionts from corals in certain environmental circumstances – on coral productivity and coral health (Venn et al., 2008). See also: Algal Symbioses; Biotic Response to Climatic Change; Cnidaria (Coelenterates); Dinoflagellates In addition to algal symbiosis among reef-building corals, autotroph–heterotroph symbioses have been detected in other ocean habitats. Among various animals inhabiting deep-sea regions near hydrothermal vents, several contain symbiotic chemosynthetic prokaryotic microbes, especially sulphur-oxidizing bacteria and methanogens. One of the most well-known of these hosts are the gutlness, mouthless vestimentiferan polychaetes; these worms provide oxygen and reduced sulphur to autotrophic sulphuroxidizing bacteria, whose chemoautotroph activities provide organic carbon to their hosts (Dubilier et al., 2008). See also: Hydrothermal Vent Communities; Marine Communities; Methanogenesis: Ecology Exceptions to the rule: However, food and nutrients are not the only currency exchanged in symbiotic transactions. For animals colonized by the bioluminescent bacterium Vibrio fischeri, for instance, light, not nutrients, is the key benefit of symbiosis for the host (Nyholm and McFallNgai, 2004). For other symbiotic mutualisms, such as fungal endophytes in plants, or bacterial symbionts of several fungal or protozoan pathogens, central benefits to hosts include such non-nutritional effects as anti-herbivore or anti-pathogen defenses, drought resistance or apparently non-nutrient based enhancement of host reproduction (Oliver et al., 2010; U’Ren et al., 2012). Although the metabolic interactions between microbial symbiosis in molgulid tunicates have been only partially characterised, the location of the symbionts within the host animals (outside the gut), the active feeding of the host and the 6 concentration of molgulid diversity in notably nutrientrich ocean waters suggests that, for these animals, the key benefits of the infection are not mainly about provision of basic organic carbon and nitrogen to the host, but perhaps lay in more specific metabolic or molecular contributions (Saffo et al., 2010). See also: Bioluminescence; Urochordata (Tunicates) GENERALISATION 2. Mutualistic symbiosis is most prevalent and/or more diverse in areas, as in many tropical ecosystems, where ‘biotic’ interspecies interactions are thought to be dominant. Symbiotic mutualisms are certainly numerous in the tropics, and many types of symbiosis show their greatest diversity there; several of them are also of major ecological importance. For instance, fungal endophytes are found at all latitudes, but are most diverse in the tropics (U’Ren et al., 2012). With the assistance of their dinoflagellate symbionts, tropical scleracticinian corals build reefs of geographical and navigational scale, forming the physical and trophic foundation of tropical marine ecosystems of unusually high productivity and species diversity. Symbiont-powered reef-building scleractinians are not only most diverse in tropical waters, but are also essentially found only in such waters. See also: Algal Symbioses; Shallow Seas Ecosystems Exceptions to the rule: However, symbiotic mutualisms are by no means limited to tropical latitudes, nor is their diversity or abundance inevitably greatest in the tropics. Though ectomycorrhizal fungi are found in the tropics, their greatest diversity is in higher latitudes (Tedersoo and Nara, 2010). Similarly, molgulid tunicates (with a symbiont prevalence of 100% in adult populations) reach their highest diversity in boreal and polar latitudes, and are almost completely absent from shallow, warm tropical oceans (Saffo et al., 2010). See also: Basidiomycota; Urochordata (Tunicates) GENERALISATION 3. Hereditarily transmitted endosymbioses favour the evolution of mutualism (mutually obligate relationships). GENERALISATION 4. Hereditarily transmitted mutualistic symbioses are more stable than horizontally-transmitted (non-hereditary) mutualisms. Among the more astonishing symbiotic mutualisms are beneficial associations between hereditarily transmitted bacteria and insect hosts, several of which serve as classic examples of extreme mutual dependence between symbionts and hosts. Aphids, for instance, feed exclusively on a nutrient-limited diet of plant phloem. Aphids also are obligately associated with the hereditarily transmitted mutualistic bacteria, Buchnera, on which they depend for provision of essential amino acids missing from plant phloem: in turn, Buchnera are themselves obligately associated with aphids. So far has the interdependency of hosts and symbionts progressed in the aphid–Buchnera symbiosis that not only metabolites, but also genomes This is a US Government work and is in the public domain in the United States of America. eLS & 2014, John Wiley & Sons, Ltd. www.els.net Mutualistic Symbioses themselves have become complementary to each other, with Buchnera possessing a dramatically reduced genome compared to its free-living relatives, but retaining pathways of use to its host. Recent genomics studies have revealed similar patterns of genome reduction and complementarity in other bacterial–insect symbioses as well (Hansen and Moran, 2014; Husnik et al., 2013; Moran et al., 2008; Shigenobu and Wilson, 2011; Wernegreen, 2005). With hereditarily transmitted symbioses, the reproductive interests of both hosts and symbionts have become inextricably linked; the mirror-image patterns of codiversification between Buchnera and aphids reinforce the notion of a shared evolutionary fate for host and symbiont clades. These characteristics, coupled with the extreme physiological interdependence of such hereditary mutualisms, have led biologists to the understandable view that hereditary symbionts are much more dependent on their hosts than horizontally transmitted mutualisms, which are often viewed as ‘facultative’ (e.g. Sachs et al., 2011). Hereditary beneficial symbioses have also been considered more ‘stable’ than their horizontally transmitted counterparts, in part because of the simple fact that the bacterial infection seems a permanent one, physically incapable of ‘divorce’. And, indeed the aphid–bacterial alliance seems to have persisted for 100–200 million years (My). In contrast, research on the complex dynamics of many horizontally transmitted mutualisms have revealed ecologically contingent, physiological fragility of mutualistic dynamics, in many such associations, most notably mycorrhizae, legume-rhizobial symbioses and some algalinvertabrate symbioses (Hoeksema et al., 2010; Sachs and Simms, 2006; Saffo, 2001). Some genomic analyses have also suggested evolutionary instability in some associations (e.g. ectomycorrhziae: Hibbett et al., 2000). See also: Mycorrhiza; Rhizobia Exceptions to the rules: But to conclude from these data that mutual interdependence and evolutionary stability occur only in hereditary mutualisms is to underestimate both the evolutionary and physiological complexity of hereditary associations and the evolutionary persistence and physiological interdependencies of many horizontally transmitted mutualisms. First of all, despite their extreme dependence, hereditarily transmitted bacteria are by no means static, either physiologically or evolutionarily, but instead (Wernegreen and Wheeler, 2009, on the symbiosis between the ant Camponotus and the bacterium Blochmannia) can still vary in density at different stages of host development; in some bacteria–insect symbioses, there is also evidence for acquisition of additional hereditary symbionts, as well as evidence of genomic change, including sometimes-rapid change, in symbionts and hosts over evolutionary time (Moran et al., 2008; Wernegreen, 2005; Wernegreen and Wheeler, 2009). In addition, many horizontally transmitted symbioses are by no means ‘facultative’ in nature. For instance, despite intensive attempts at axenic laboratory culture of these ecologically and agriculturally important fungi, arbuscular mycorrhizal fungi can only reproduce in association with a plant host. With the exception of a resistant spore stage that can survive for a time in seawater, the rest of the complex life cycle of the apicomplexan symbiont Nephromyces occurs only within its hosts (Saffo et al., 2010). Termites and their horizontally transmitted gut symbionts have clear, mutually obligate physiological dependence on each other. See also: Mycorrhiza Third, despite the physiological complexities of horizontally transmitted mutualisms, the supposedly ‘facultative’, ‘unstable’ mutualisms such as arbuscular mycorrhizae have a remarkably long evolutionary history, not only sticking with their terrestrial plant partners for more than 400 My, but so linked to the earliest evolution of plants, that they are essentially a defining feature of the embryophyta (vascular plants, ferns and mosses; Bonfante and Selosse, 2010; Rodriguez and Redman, 2008; Wang et al., 2010). Similarly, biologists have described lichen-like fossils from rocks 400–600 My old (Rikkinen and Poinar, 2008). Reef-building corals have been on earth, presumably in partnership with algal symbionts, for at least 200 My. Among examples of mutualisms with lower physical connections, leaf-cutter ants have been cultivating their fungal ‘gardens’ for 50 My (Suen and Currie, 2008). The extraordinary persistence of such horizontally transmitted mutualisms despite their once-or-more-a-generation opportunities for ‘divorce’, reminds us once again of the improbability of such associations, and of how much we still need to learn about the physiological processes and ecological forces that have maintained and renewed these partnerships for so much of the history of life. See also: Mutualism Among Free-living Species; Plant–Fungal Interactions in Mycorrhizas Do Immune Defenses Keep Mutualisms Together? The Importance of Partner Choice Theoretical biologists continue to grapple with the question of what keeps mutualisms mutualistic, and, indeed, what keeps the partnerships together at all (Kiers and van der Heijden, 2006). Central to much thinking is that the partners are in it for the benefits: when benefits or need disappears, many horizontally-transmitted mutualisms (for instance, symbioses of legumes with nitrogen-fixing bacteria, or plants with mycorrhizal fungi in fertilised soil) can shift into a parasitic direction, or fall apart altogether; also, as reviewed earlier, a number of symbioses can change from mutualistic to parasitic simply with a change in host or symbiotic partners. Focusing on the importance of benefits, several analyses (e.g. Sachs and Simms, 2006; Kiers et al., 2011) have emphasised the importance of hosts punishing potential ‘cheaters’: symbionts who take advantage of room and board in or on their host, with no payment of metabolites in return. Other thoughtful recent analyses have emphasised the importance of partner This is a US Government work and is in the public domain in the United States of America. eLS & 2014, John Wiley & Sons, Ltd. www.els.net 7 Mutualistic Symbioses fidelity (Weyl et al., 2010, 2011) in evolution of optimally mutualistic symbioses. The former approach could be criticised for focusing perhaps too much attention on host control, and not enough attention on the influence of symbionts on their hosts; the latter approach could be criticised for not accounting for the several cases of evolutionarily and ecologically robust mutualisms that involve multiple symbiotic partners or promiscuous partnerships. As a way to bridge the differing perspectives, it seems reasonable to think that the mechanisms and selective forces keeping mutualisms together might be different for different mutualisms. But it is also worthwhile pointing out that central to both classes of models is the importance of partner choice. Several studies suggest that immune defences, so paradoxically at odds with the evolution and tolerance of beneficial infections, may in fact play an important role in symbiotic partner choice, that is, in influencing the establishment and tolerance of beneficial infections. In reviewing the plant responses to rhizobial infection, Soto et al. (2009) note that, in legumes, both plant pathogens and rhizobia are initially perceived as intruders, but, in the case of rhizobial infection, those defence responses are apparently localised and transient, possibly because (and a reminder that the host is not necessarily the only partner in control of the interaction) the rhizobia themselves may play some role in suppression of host defences. Similar dynamics have also been described in mycorrhizal plant colonisation as well. 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