…the Kudzu bug (Megacopta cribraria), an agricultural pest, is born without any symbionts. After birth it acquires a specific symbiont from bacterial capsules left by its mother. If these capsules are removed, the bugs show dramatic wandering behaviors, presumably to search for symbiont capsules left with nearby eggs . — Vanessa O. Ezenwa et al. (2012)

Symbioses are products of coevolution. Coevolution can be viewed as a situation where modification of one organism or organism part selects for modification of another. To some degree the idea of coevolution is muddled by the potential for adaptations to represent responses to modifications of more than one organism, such as increases in the running speed of multiple prey species selecting for increases in running speed in perhaps multiple predator species. With symbioses, however, the concept of coevolution truly can involve one species responding evolutionarily to another. Indeed, in terms of mutualisms involving microorganisms, to the extent that the microorganism (one or more) has specialized toward interacting with a particular host species, that symbiont probably has evolved to optimize those interactions, and likely has done so at the expense of its potential to similarly interact with other host species (which would imply that such coevolution, at least by the symbiont, could serve as yet another example of antagonistic pleiotropy).

Key to specialization by symbionts is some kind of reproductive linkage between the organisms making up the symbiosis. This linkage can be simply geographical, though the potential for the symbiosis to be a mutualism probably increases the closer such linkage is tied to host reproduction, i.e., "co-vertical transmission" of the symbiosis, where for example a mother's symbionts are passed down to the mother's progeny. This argument is similar to that for why cooperation is more likely given long-term versus more short-term associations. Indeed, mutualisms can viewed explicitly as a kind of intra-specific cooperation.

Symbioses among microorganisms typically involve some kind of chemical exchange where one partner either supplies nutrients or sequesters waste from the other partner, and vice versa (i.e., syntrophy). This can be seen also between microbes and macrobes, where microbes often also are supplied with protection and a place to live by the larger organism. Such interactions can progress to an absolute dependence by both organisms on the symbiotic relationship. In those cases, schemes by which co-vertical transmission may occur with high likelihood typically evolve. Such co-vertical transmission is seen with endosymbioses where the symbiotic organism is segregated in the course of cell division as though it were an organelle. At an extreme, symbiotic relationships involve the merging of genomes. Variations on the symbiosis theme are described below with endosymbiosis considered in the subsequent section.

Microbe-Macrobe Symbioses

Symbioses between larger organisms and microorganisms are abundant, such as microorganism symbioses with animals or plants. Many of these symbioses, in fact, are endosymbioses, some of which are more permanent (involving co-vertical inheritance) while others are less permanent, requiring host organism re-acquisition of the symbiotic organism each generation. In this section I emphasize these less-permanent symbiotic relationships, ignoring for the moment those symbioses that are both permanent and endosymbiotic.

Microbe-macrobe symbioses are almost absurdly common, with each species, indeed, perhaps even each individual member of a species, carrying around with them a unique microbiome that often greatly exceeds, especially in terms of cell number, the size of the host organism itself. Most of these organisms we typically described as normal flora. Most normal flora may be beneficial to the carrying organism, though the impact of many flora members may be redundant to the impact of other members. Thus, it can be difficult to conceptualize these symbioses as mutualisms since it can be difficult to prove that benefits actually accrue from the presence of a given species of microorganism. On the other hand, it can be hard to selectively remove individual species, resulting in difficulties in demonstrating any low-level beneficial or deleterious impacts on a host coming from specific normal flora species. Nonetheless, there also exist a number of host-flora relationships for which specific and non-redundant benefits are accrued by the host, and these more-easily demonstrated mutualisms are what I concentrate on here.

Variously, such microbe-macrobe symbioses include the algae-fungi mutualism that makes of lichens, where fungi (the macrobe) supply water, nutrients, and protection while the algae (the microbe) supply photosynthetic products. Similarly, mycorrhizal fungi can be found in symbiotic relationships with plant roots, again with the plants playing the role of autotroph (and, here, also as the macrobe) and the fungi (now the microbe) playing the role of nutrient gatherers. Plants even can be protected by vertically inherited fungi and bacteria (Selosse et al., 2004) . Protective microorganisms can also be found in association with insects . Indeed, microbial antagonism is thought to be a common feature among normal flora where an otherwise benign organism taking up space, utilizing nutrients, and/or producing antimicrobial products including antibiotics can protect hosts from other organisms, such as from pathogenic bacteria.

Nitrogen-fixing bacteria, rhizobia, are found in the root nodules of certain plants. Various luminescent bacteria are found in association with sea animals (e.g., squid), providing their light organs with light. There are also marine worms that gather nutrients from chemolithotrophic bacteria found within them as symbionts (these worms, e.g., are found in the vicinity of deep sea hydrothermal vents). Corals, too, have symbiotic photosynthetic algae, in a relationship that presumably is analogous to that of the fungal-algae relationship in lichen. Termites have Trichonympha protists which contribute to the digestion of the wood the termites ingest. In fact many animals possess symbiotic organisms that contribute to food digestion, such as the digestion of cellulose by ruminants (e.g., cows), or even the digestion of cellulose by primates in their large intestine. In any case, for a symbiosis to truly represent a symbiosis, the microorganism must remain capable of reproducing in the course of the relationship, since otherwise the symbiont may be viewed instead as slave or slowly assimilated food, or both! Note that even microbe-microbe symbioses occurring within the context of microbe-macrobe symbioses are not uncommon (see following section). From Selosse et al. (2004) (abstract):

Plant-associated microbial diversity encompasses symbionts, protecting their host against various aggressions. Mycorrhizal and rhizospheric microorganisms buffer effects of soil toxic compounds and soil-borne pathogens. Endophytic bacteria and fungi, some of which are vertically inherited through seeds, take part in plant protection by acting directly on aggressive factors (mainly pathogens and herbivores) or by enhancing plant responses. Plant protective microbial symbionts determine the ecological success of plants; they drastically modify plant communities and related trophic webs.

Microbe-Microbe Symbioses

Perhaps because they are either less obvious, less common, or of less interest economically, there are fewer described examples of microbe-microbe symbioses than of ones between microbes and macrobes. Of those that are known between cellular microorganisms, they can be differentiated into what can be described as microbial consortia, other symbiotic or symbiosis-like interactions that nevertheless are more casual (i.e., less coevolved), and endosymbioses. In this section I emphasize microbial consortia first. In the subsequent section I discuss endosymbioses, the latter of both microbes and macrobes. Note that it is also possible to have microbe-microbe symbioses that occur between cellular organisms and their acellular components, e.g., as may involve prophages and lysogenic conversion or various useful traits expressed by plasmids, though these will not be an emphasis of this chapter.

Microbial Consortia

What we understand to be the 'individual' develops as a consortium of animal cells and microbes… — Scott Gilbert as quoted in (Pennisi, 2013)

A microbial consortium is a physically associated collection of microorganisms that synergistically interact, i.e., by exchanging chemicals. As such they can be viewed as a form of presumably coevolved (at least in some instances) symbiotic or symbiosis-like interactions between two or more microbial species. In their metabolic integration, they are analogous to the metabolic differentiation that can be observed with multicellular organisms, except that in the case of microbial consortia the cells are not clonally related but instead owe their different metabolism to different genotypes. Nonetheless, metabolisms can be so closely linked that it can be difficult to distinguish consortia into multiple species, except through molecular typing, just as it is difficult to appreciate that lichens consist of multiple species, except, in that case, via microscopic observation. The importance of microbial consortia lies not just in that they represent an interesting form of microbial life/evolution, but also because they potentially are evolutionary forerunners of the eukaryotic cell, at least according to certain hypotheses, and/or forerunners to early endosymbioses such as the acquisition of mitochondria.

Various microbial consortia have been described. For example, methane hydrates in marine sediments have associated consortia consisting of methane-oxidizing Archaea surrounded by sulfate-reducing Bacteria (Hoffmeister and Martin, 2003) . Another example is a consortium, dubbed Chlorochromatium aggregatum, which consists of a central heterotrophic organism surrounded by photosynthetic bacteria (Searcy, 2003) . Theoretically, the heterotrophic organism supplies reduced sulfur (H2S) to the photosynthetic organisms, along with oxidized carbon (CO2), which together are employed in a sulfur-based, anaerobic photoautotrophic metabolism. The photosynthetic bacteria return oxidized sulfur (S0) along with reduced carbon (i.e., organic molecules), which represent electron acceptor and electron donor in anaerobic cellular respiration, respectively. That is, photons supply the energy that drives an ongoing recycling of electron carriers. Note that this consortium may be more complicated than just two species living closely together, as reviewed by Lake (2009) (p. 967):

… 'Chlorochromatium aggregatum' …consists of two partners; a motile, heterotrophic, central β-proteobacterium surrounded by 10-60 peripheral photosynthetic green sulphur bacteria (Fröstl and Overmann, 2000) . The green sulphur bacteria, or epibionts… are attached to the central bacterium through periplasmic tubules formed by extensions from the outer membrane of the flagellated central β-proteobacterium. This allows the central β-proteobacterium… to move the consortium to favourable anaerobic habitats where sulphides and sufficient light for photosynthesis are available. Structural studies of the consortium suggest that, ''the two partner bacteria may actually share a common periplasmic space'' (Wanner et al., 2008) . . If so, then both partners would be enclosed by a common periplasm, but not by a common membrane. Although this symbiosis does not provide a precedent for a prokaryotic endosymbiosis, it suggests how one might have started.

Consortia also can be found in association with animals. One such consortium appears to exist within a gutless worm, Olavius algarvensis (Hoffmeister and Martin, 2003) . Here one consortium member, a chemoautotroph, supplies the worm host with organic molecules (carbohydrate) which are generated from CO2 and sulfide, i.e., S2-. The sulfide comes from the other consortium member, which is either chemoorganotrophic or chemolithotrophic, that is, obtaining its energy either from H2 (in this case) or from organic carbon. Apparently only one of these bacteria is capable of supplying the worm with chemical energy, but itself is not able to fix carbon without the sulfide from the second organism, which in turn can get its energy from hydrogen gas, an energy source that otherwise is not available to the worm.

There exists at least one pathogenic condition that has been described as having a microbial consortium etiology, black band disease of coral. This consortium consists of a combination of photosynthetic and non-photosynthetic bacteria and appears to represent sulfur oxidation-reduction pairs, plus the cyanobacteria, as may similarly be found in illuminated, sulfide-rich microbial mats. The diversity of the black bands can be greater than just these three members, however. There likely are more microbial consortiums that give rise to disease but which are recognized as mixed-etiology infections instead. That is, infectious diseases that might have more than microbial etiology associated with it, but otherwise (generally) have not been well-studied to determine the contributions of various member organisms to the overall disease process.


Loading