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Springer MRW: [AU:, IDX:] I Intestinal Symbionts symbionts are best known from termites, but they are found across the social insects (Fig. 1). Corrie S. Moreau Departments of Entomology and Ecology and Evolutionary Biology, Cornell University, Termites Ithaca, NY, USA Termite gut symbionts contain members from all three domains of life (Archaea, Bacteria, and Synonyms Eukarya). Termites exhibit different ▶ feeding syndromes, with diets comprising lignocellulose Gut biome; Gut fauna; Gut symbionts; Intestinal (cellulose and lignin) plant material including biome; Intestinal fauna wood, various stages of decaying plant material, animal dung, and soil rich in organic material. As Host-microbe interactions are ubiquitous termites, like almost all other animals, cannot across the tree of life and can range from mutual- digest these food sources and these food sources istic to parasitic. In social insects, a diversity of are limited in their nutritional quality and host-associated microbes has been identified, access, intestinal symbionts are responsible for including maternally transmitted bacteria that the breakdown of cellulose and for nitrogen acqui- selfishly manipulate the host’s reproduction to sition [1, 2]. In fact, termites that have had their cuticular bacteria that help fungus-gardening gut symbionts removed, but are otherwise healthy, ants in the fight against parasitic fungi. Although die even in the presence of ample wood or microbes can be found in many places on and in cellulose. the host, the majority of symbiotic microbes are The two major groups of termites host different associated with the digestive tract. Symbiotic extracellular gut community members. The lower microbes in the intestinal tract can benefit the termites host dense communities of Bacteria, host through a myriad of ways, including nutri- Archaea, and flagellate protozoa, many of which tional upregulation, defense from pathogens and host their own prokaryotic symbionts, while the parasites, and by increasing environmental toler- higher termites have diverse bacterial gut commu- ance [4]. Internal microbial communities can not nities, but almost always lack protozoa. In the only provide immediate ecological benefits to the lower termites, the protozoa are primarily respon- host but in some cases may even benefit the host sible for the degradation of cellulose into digest- on an evolutionary scale. Gut microbial ible sugars, which are then converted into short-chain fatty acids. In the higher termites, in © Springer Nature Switzerland AG 2020 C. Starr (ed.), Encyclopedia of Social Insects, https://doi.org/10.1007/978-3-319-90306-4_65-1 2 Intestinal Symbionts Intestinal Symbionts, Fig. 1 Gut microbial symbionts have been documented and studied in several social insect groups including termites, cockroaches, social aphids, bees, and ants. (Photos by Alex Wild) contrast, lignocellulose moves through various to feed on an abundant food source that is specialized gut chambers where it is decomposed undigestible to most of life, which may account through chemical processes. The gut-associated for their high abundance in many ecosystems. bacteria are responsible for providing nitrogen to the host primarily through N-fixation, although recycling of uric acid has also been observed. ▶ Wood-Feeding Cockroaches During these digestive processes, a major product is methane gas, and termites are considered a A close phylogenetic relationship between cock- major contributor of methane in our atmosphere. roaches and termites was first suggested by These microbial communities are not evenly the observation that wood-eating cockroaches distributed across the digestive tract. Although (▶ Cryptocercus) harbor a similar fauna of gut there are some bacteria associated with the foregut flagellates. It is now accepted that termites are a and midgut, the majority of the intestinal micro- special group of social cockroaches, with biota are found in the hindgut. As these microbial Cryptocercus as their sister group. The latter’s communities are extracellular and not strictly intestinal communities comprise bacteria and pro- maternally transmitted, termites must acquire tozoans which enable them to digest cellulose. these essential symbionts through behavioral Gut microbial symbionts in some other cockroach transmission. This is primarily accomplished species are responsible for the production of pher- through oral-anal ▶ trophallaxis. Associations omones secreted in the feces, which serve as with intestinal symbionts have permitted termites aggregation cues. Intestinal Symbionts 3 ▶ Social Aphids some species are found predominately in the rec- tum. The gut microbiota of honey bees has been Social aphids are plant-feeding hemipterans that shown to increase body weight gain and confer rely on an obligate nutrient-provisioning bacte- resistance to ▶ pathogens. Additionally, one of rium, Buchnera aphidicola [3, 5]. These bacteria the most notable roles of the honey bee gut com- are housed in host-derived bacteriocyte cells and munity is that these bacteria likely permit their are maternally transmitted through the egg. These hosts to digest pollen. bacteriocytes are aggregated into specialized Along with honey bees, ▶ bumble bees also organs called bacteriomes that are located near appear to have a stable, socially transmitted the host’s midgut. This obligate intracellular (through interactions with other members of the endosymbiont has been co-diversifying with its colony or direct contact with the nest substrate), aphid hosts for 150–250 million years. Buchnera and functionally important gut bacterial commu- produce essential amino acids for their insect host. nity that overlaps in some of its core components As this bacterium is found only within aphid with that of honey bees. As in honey bees, the gut hosts, it has lost many of the genes required for bacterial community of bumble bees also protects free-living and has one of the smallest genomes the host from parasitic infections. recorded. There is also a range of facultative microbes that have been found associated with aphids that Ants often provide benefits to the host in specific eco- logical contexts. For example, the maternally Although we know many details about the gut- transmitted bacterium, Hamiltonella defensa, pro- associated microbial community for individual tects aphids from parasitoids by causing mortality social insects, in the ants we have a better under- of parasitoid larvae. Two other facultative bacte- standing of the diversity of host-associated ria, Regiella insecticola and Serratia symbiotica, microbes across many species [6]. Ants have a also provide protection against these natural ene- great diversity of diets, with some species being mies. In addition to its role in protection from entirely predatory, others having strict fungal- or parasitoids, S. symbiotica has also been shown to plant-derived diets, while the majority are omni- protect aphids from the detrimental effects of heat vores. This provides the opportunity to investigate stress, an example of host-associated microbes the role of gut microbial communities and host increasing environmental tolerance for the host. diet in a comparative framework. The best-studied Interestingly, although these facultative bacteria gut-bacterial interactions among the ants comes are maternally transmitted, they are found at var- from the ▶ carpenter ants (Camponotus), ▶ spiny iable frequencies in natural populations of the host ants (Polyrhachis), and their close relatives. aphid. This suggests that there is a net cost to In this ancient symbiosis, maternally transmit- maintaining the symbiosis if the ecological pres- ted intracellular bacteria from the genus sure is not high. Blochmannia have been co-diversifying with their ant hosts for over 40 million years. This midgut-associated bacterium resides in Bees bacteriocytes and supplements the host’s nutrition through nitrogen recycling and amino acid syn- ▶ Honey bees are the most thoroughly studied of thesis. To date the majority of gut-associated all insects, and, not surprisingly, the majority of microbes have been shown to be extracellular what we know about bee gut-associated micro- and, as in termites, these microbial communities biomes comes from honey bees. Their intestinal are not evenly distributed throughout the digestive tracts contain a distinctive, yet relatively simple tract. For ants feeding low on the trophic scale, community of bacteria of only a few species. The there appear to be multiple independent origins of majority of these bacteria reside in the ileum, but putative nutrient-provisioning bacteria. Bacteria 4 Intestinal Symbionts Intestinal Symbionts, Fig. 2 The digestive tract of a turtle ant (Cephalotes varians) showing the distinct comparts. Typically, the crop, or social stomach, does not seem to harbor a persistent functional bacterial community, while the midgut, ileum, and rectum have all been shown to harbor diverse and stable gut communities with functional roles for the host of the order Rhizobiales have been shown to be transmission mechanisms among individuals. associated with a diversity of distantly related Social interactions provide opportunities for the ants, including Cataulacus, Cephalotes, transmission of gut microbial communities, which Dolichoderus, and Tetraponera. Among the may explain the diversity, stability over evolution- ▶ turtle ants (Cephalotes), the gut-associated bac- ary time, and functional importance of gut- terial community is stable, has been co-evolving associated microbes
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