Access to mutualistic endosymbiotic microbes: an underappreciated benefit of group living

Lombardo, Michael P.

doi:10.1007/s00265-007-0428-9

Cited by 176 publications

(174 citation statements)

References 193 publications

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“…Socialization and other interactions between these species are known to occur and could increase the potential for microbial transmission, thereby contributing to the richness of South Australian sea lion gut microbiota (42). Similar findings have been reported in studies observing southern elephant and leopard seal gut microbiota.…”

Section: Discussionsupporting

confidence: 84%

Colony Location and Captivity Influence the Gut Microbial Community Composition of the Australian Sea Lion (Neophoca cinerea)

Delport

Power

Harcourt

et al. 2016

Appl Environ Microbiol

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Gut microbiota play an important role in maintenance of mammalian metabolism and immune system regulation, and disturbances to this community can have adverse impacts on animal health. To better understand the composition of gut microbiota in marine mammals, fecal bacterial communities of the Australian sea lion (Neophoca cinerea), an endangered pinniped with localized distribution, were examined. A comparison of samples from individuals across 11 wild colonies in South and Western Australia and three Australian captive populations showed five dominant bacterial phyla: Firmicutes, Proteobacteria, Bacteroidetes, Actinobacteria, and Fusobacteria. The phylum Firmicutes was dominant in both wild (76.4% ؎ 4.73%) and captive animals (61.4% ؎ 10.8%), while Proteobacteria contributed more to captive (29.3% ؎ 11.5%) than to wild (10.6% ؎ 3.43%) fecal communities. Qualitative differences were observed between fecal communities from wild and captive animals based on principal-coordinate analysis. SIMPER (similarity percentage procedure) analyses indicated that operational taxonomic units (OTU) from the bacterial families Clostridiaceae and Ruminococcaceae were more abundant in wild than in captive animals and contributed most to the average dissimilarity between groups (SIMPER contributions of 19.1% and 10.9%, respectively). Differences in the biological environment, the foraging site fidelity, and anthropogenic impacts may provide various opportunities for unique microbial establishment in Australian sea lions. As anthropogenic disturbances to marine mammals are likely to increase, understanding the potential for such disturbances to impact microbial community compositions and subsequently affect animal health will be beneficial for management of these vulnerable species. IMPORTANCEThe Australian sea lion is an endangered species for which there is currently little information regarding disease and microbial ecology. In this work, we present an in-depth study of the fecal microbiota of a large number of Australian sea lions from geographically diverse wild and captive populations. Colony location and captivity were found to influence the gut microbial community compositions of these animals. Our findings significantly extend the baseline knowledge of marine mammal gut microbiome composition and variability. It is predicted that global change will have many major, but as yet unknown, impacts on aquatic ecosystems. Marine mammal species, including bottlenose dolphins, sea otters, manatees, and gray whales, have been proposed as sentinels for diverse threats to aquatic health, including disease transmission, changes in food webs, and contaminant levels (1-6). The key roles and contributions of microbes to mammalian host health are becoming increasingly recognized, yet remain largely unexplored for marine mammals (7). An understanding of the impacts of anthropogenic pressures on marine mammal microbial communities and of the potential cascade of impacts on marine health is necessary for full exploration of the roles a...

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Section: Discussionsupporting

confidence: 84%

Colony Location and Captivity Influence the Gut Microbial Community Composition of the Australian Sea Lion (Neophoca cinerea)

Delport

Power

Harcourt

et al. 2016

Appl Environ Microbiol

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“…These behaviours can facilitate exchange of microbes among nest members, thereby contributing to maintenance of a beneficial microbiota, as has been demonstrated in ants [16,28,29], termites [30] and bees [31,32]. In fact, it has been speculated that the evolution of complex social forms could be reinforced, among other factors, by the convenience of acquiring beneficial microbes through recurring contact with conspecifics [33]. Recent examination of the gut microbiota of different bee species suggests that sociality plays an integral role in maintenance of the distinctive microbial communities within the Apoidea superfamily [31,34].…”

Section: (C) Social Acquisitionmentioning

confidence: 95%

An out-of-body experience: the extracellular dimension for the transmission of mutualistic bacteria in insects

et al. 2015

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Across animals and plants, numerous metabolic and defensive adaptations are a direct consequence of symbiotic associations with beneficial microbes. Explaining how these partnerships are maintained through evolutionary time remains one of the central challenges within the field of symbiosis research. While genome erosion and co-cladogenesis with the host are well-established features of symbionts exhibiting intracellular localization and transmission, the ecological and evolutionary consequences of an extracellular lifestyle have received little attention, despite a demonstrated prevalence and functional importance across many host taxa. Using insect-bacteria symbioses as a model, we highlight the diverse routes of extracellular symbiont transfer. Extracellular transmission routes are unified by the common ability of the bacterial partners to survive outside their hosts, thereby imposing different genomic, metabolic and morphological constraints than would be expected from a strictly intracellular lifestyle. We emphasize that the evolutionary implications of symbiont transmission routes (intracellular versus extracellular) do not necessarily correspond to those of the transmission mode (vertical versus horizontal), a distinction of vital significance when addressing the genomic and physiological consequences for both host and symbiont.

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“…With regard to social insects, group living can facilitate the transmission of not only parasites (10) but also beneficial microbes (11). Adult honey bees and bumble bees have recently been shown to harbor a specialized and surprisingly species-poor community of bacteria in their gut (12,13).…”

mentioning

confidence: 99%

Socially transmitted gut microbiota protect bumble bees against an intestinal parasite

Koch

Schmid‐Hempel

2011

Proc. Natl. Acad. Sci. U.S.A.

712

702

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Populations of important pollinators, such as bumble bees and honey bees, are declining at alarming rates worldwide. Parasites are likely contributing to this phenomenon. A distinct resident community of bacteria has recently been identified in bumble bees and honey bees that is not shared with related solitary bee species. We now show that the presence of these microbiota protects bee hosts against a widespread and highly virulent natural parasite ( Crithidia bombi ) in an experimental setting. We add further support to this antagonistic relationship from patterns found in field data. For the successful establishment of these microbiota and a protective effect, exposure to feces from nest mates was needed after pupal eclosion. Transmission of beneficial gut bacteria could therefore represent an important benefit of sociality. Our results stress the importance of considering the host microbiota as an “extended immune phenotype” in addition to the host immune system itself and provide a unique perspective to understanding bees in health and disease.

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Access to mutualistic endosymbiotic microbes: an underappreciated benefit of group living

Cited by 176 publications

References 193 publications

Colony Location and Captivity Influence the Gut Microbial Community Composition of the Australian Sea Lion (Neophoca cinerea)

Colony Location and Captivity Influence the Gut Microbial Community Composition of the Australian Sea Lion (Neophoca cinerea)

An out-of-body experience: the extracellular dimension for the transmission of mutualistic bacteria in insects

Socially transmitted gut microbiota protect bumble bees against an intestinal parasite

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