Extended mutualism between termites and gut microbes: nutritional symbionts contribute to nest hygiene

Inagaki, Tatsuya; Matsuura, Kenji

doi:10.1007/s00114-018-1580-y

Cited by 12 publications

(9 citation statements)

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“…Overall our study provides evidence that swallowing of formic acid containing poison gland secretions acts as a chemical filter for microbial selection and control of gut associated microbes, protecting formicine ants from food borne bacterial pathogens and structuring gut associated microbial communities. In ants and other animals that lack acidic poison gland secretions, acids produced by other exocrine glands (Fernández-Marín et al, 2015, Yek and Mueller, 2011) or acidic derivatives produced by defensive symbionts (Florez et al, 2015) or other environmental bacteria (Ratzke and Gore, 2018) might provide functionally similar roles to acidic poison gland secretions, as indicated in bees (Palmer-Young et al, 2018) and termites (Inagaki and Matsuura, 2018). Antimicrobials as external immune defence traits (Otti et al, 2014) may generally not only serve pathogen protection and microbial control but may also act as microbial filters to manage host associated microbes, be it in food or the environment, and thus contribute to a host’s ecological and evolutionary success.…”

Section: Resultsmentioning

confidence: 99%

Formicine ants swallow their highly acidic poison for gut microbial selection and control

Tragust

Herrmann

Häfner

et al. 2020

Preprint

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12Animals continuously encounter microorganisms that are essential for health or cause disease. 13 They are thus challenged to control harmful microbes while allowing acquisition of beneficial 14 microbes, a challenge that is likely especially important concerning microbes in food and in 15 animals such as social insects that exchange food among colony members. Here we show that 16 formicine ants actively swallow their antimicrobial, highly acidic poison gland secretions 17 after feeding. The ensuing creation of an acidic environment in the stomach, the crop, 18 improves individual survival in the face of pathogen contaminated food and limits disease 19 transmission during mutual food exchange. At the same time, crop acidification selectively 20 allows acquisition and colonization by known bacterial gut associates. The results of our 21 study suggest that swallowing of acidic poison gland secretions acts as a microbial filter in 22 formicine ants and indicate a potentially widespread but so far underappreciated dual role of 23 antimicrobials in host-microbe interactions. 24 25 85 5 experimental manipulation of poison gland access, and behavioural observations. In loss of 86 poison gland function experiments, we then investigate whether analogous to acidic stomachs 87 of higher vertebrates and acidic midgut regions in the fruit fly, swallowing of poison gland 88 substances can serve gut microbial control and prevent bacterial pathogen infection and 89 transmission. Finally, we explore whether swallowing of poison gland substances acts as a 90 microbial filter that is permissible to gut colonization of bacteria from the family 91 Acetobacteracea. 92 93 Results and Discussion 94To reveal whether poison gland secretions are swallowed during acidopore grooming, we 95 monitored acidity levels in the crop lumen of the Florida carpenter ant Camponotus floridanus 96 at different time points after feeding them 10% honey water (pH = 5). We found that over 97 time, the crop lumen became increasingly acidic, reaching highly acidic values 48h after 98 feeding (median pH = 2; 95% CI: 1.5-3.4), whilst renewed access to food after 48h restored 99 the pH to levels recorded after the first feeding trial ( Fig. 1a; LMM, LR-test, χ 2 = 315.18, df = 100 3, P < 0.001; Westfall corrected post-hoc comparisons: 0+4h vs. 48h+4h: P = 0.317, all other 101 comparisons: P < 0.001). This acidification was limited to the crop and did not extend to the 102 midgut (Fig. 1figure supplement 1; pH-measurements at four points along the midgut 24h 103 after access to 10% honey-water; mean ± se; midgut position 1 = 5.08 ± 0.18, midgut position 104 2 = 5.28 ± 0.17, midgut position 3 = 5.43 ± 0.16, midgut position 4 = 5.31 ± 0.19). Prevention 105 of acidopore grooming in C. floridanus ants for 24h after feeding resulted in a significantly 106 diminished acidification of the crop lumen (Fig. 1b; LMM, LR-test, χ 2 = 44.68, df = 1, P < 107 0.001), a result that was invariably obtained in a comparative survey across seven formicine 108 ant species (g...

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Section: Resultsmentioning

confidence: 99%

Formicine ants swallow their highly acidic poison for gut microbial selection and control

Tragust

Herrmann

Häfner

et al. 2020

Preprint

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“…Colonization of tsetse flies (Glossina morsitans morsitans) with the bacterium Kosakonia cowanii leads to the acidification of the midgut, inhibits proliferation of trypanosomes (the causative agents of human sleeping sickness) and increases host survival after infection with Serratia marcescens (Weiss et al, 2019). Likewise, acetate production by the gut microbiota of the dampwood termite Zootermopsis nevadensis also provides resistance to S. marcescens (Inagaki and Matsuura, 2018), and in honey bees, the same pathogen is suppressed in the presence of a normal microbiota (acidifying the gut environment) (Raymann et al, 2017;Raymann et al, 2018). Colonization resistance against the trypanosomatid pathogen Critidia bombi in bumble bees may also be mediated by the capability of the microbiota to modulate the pH (Koch and Schmid-Hempel, 2011;Koch and Schmid-Hempel, 2012): two recent studies have identified bacteria that inhibit the growth of Crithidia in vitro (Praet et al, 2018;Palmer-Young et al, 2019), and in one of them it was shown that the acidification of the culture medium is sufficient to mediate the inhibitory effect (Palmer-Young et al, 2019).…”

Section: Colonization Resistance Against Pathogensmentioning

confidence: 99%

Mechanisms underlying gut microbiota–host interactions in insects

Schmidt

Engel

2021

Journal of Experimental Biology

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Insects are the most diverse group of animals and colonize almost all environments on our planet. This diversity is reflected in the structure and function of the microbial communities inhabiting the insect digestive system. As in mammals, the gut microbiota of insects can have important symbiotic functions, complementing host nutrition, facilitating dietary breakdown or providing protection against pathogens. There is an increasing number of insect models that are experimentally tractable, facilitating mechanistic studies of gut microbiota–host interactions. In this Review, we will summarize recent findings that have advanced our understanding of the molecular mechanisms underlying the symbiosis between insects and their gut microbiota. We will open the article with a general introduction to the insect gut microbiota and then turn towards the discussion of particular mechanisms and molecular processes governing the colonization of the insect gut environment as well as the diverse beneficial roles mediated by the gut microbiota. The Review highlights that, although the gut microbiota of insects is an active field of research with implications for fundamental and applied science, we are still in an early stage of understanding molecular mechanisms. However, the expanding capability to culture microbiomes and to manipulate microbe–host interactions in insects promises new molecular insights from diverse symbioses.

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“…Herbivorous ants maintain gut bacteria that offset host dietary and metabolic limitations through amino acid supplementation, nitrogen recycling, and catabolism of glucose and citrate (Russell et al, 2009;Hu et al, 2018;Sapountzis et al, 2018). Gut microbes also contribute to disease defense in bees and termites by imparting pathogen colonization resistance (Koch and Schmid-Hempel, 2011;Peterson and Scharf, 2016;Raymann et al, 2017;Inagaki and Matsuura, 2018), further enabling host persistence and resource acquisition across environments.…”

Section: Introductionmentioning

confidence: 99%

Synergies Between Division of Labor and Gut Microbiomes of Social Insects

et al. 2020

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Social insects maximize resource acquisition and allocation through division of labor and associations with microbial symbionts. Colonies divide labor among castes and subcastes, where the plasticity of caste roles decreases in clades with higher social grades. Recent studies indicate that specific castes may also foster distinct gut microbiomes, suggesting synergies between division of labor and symbiosis. The social organization of a colony potentially partitions evolutionary persistent microbial partners to optimize symbioses and complement division of labor. However, research in this area has received limited attention. To elucidate if a structured microbiota is adaptive, we present three testable predictions to address consistent community structure, beneficial functions, and selection for microbiota that support caste roles. First, we posit that social insect groups spanning lower to higher social grades exhibit increasingly distinct caste microbiomes, suggesting that structured microbiomes may have evolved in parallel to social complexity. Second, we contend that the development of these microbiomes during colony maturation may clarify the extent to which they support division of labor. Third, we predict that mature social insect colonies with the most extreme division of labor demonstrate the strongest distinctions between caste microbiomes, carrying the greatest promise of insight into microbiome composition and function. Ultimately, we hypothesize that caste-specific microbiomes may enhance symbiotic benefits and the efficiency of division of labor, consequently maximizing fitness.

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Extended mutualism between termites and gut microbes: nutritional symbionts contribute to nest hygiene

Cited by 12 publications

References 58 publications

Formicine ants swallow their highly acidic poison for gut microbial selection and control

Formicine ants swallow their highly acidic poison for gut microbial selection and control

Mechanisms underlying gut microbiota–host interactions in insects

Synergies Between Division of Labor and Gut Microbiomes of Social Insects

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