<i>Oecophyllibacter saccharovorans</i>gen. nov. sp. nov., a bacterial symbiont of the weaver ant<i>Oecophylla smaragdina</i>

Chua, Kek Heng; See-Too, Wah-Seng; Tan, Jia-Yi; Song, Sze-Looi; Yong, Hoi-Sen; Yin, Wai‐Fong; Chan, Kok‐Gan

doi:10.1101/2020.02.15.950782

Cited by 2 publications

(3 citation statements)

References 71 publications

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“…We found that, compared to a bacterial pathogen, a bacterial member of the Acetobacteraceae was not only better able to withstand acidic conditions created with formic acid in vitro but was able to establish itself in the midgut of formicine ants in vivo. This suggests that host filtering of microbes ( Mazel et al, 2018 ) via acidic crop lumens might explain at least part of the recurrent presence of Acetobacteraceae in the gut of formicine ants and the otherwise reduced microbial diversity and abundance of gut-associated microbes in formicine ants ( Brown and Wernegreen, 2016 ; Brown and Wernegreen, 2019 ; Chua et al, 2018 ; Chua et al, 2020 ; Ivens et al, 2018 ; Russell et al, 2017 ).…”

Section: Discussionmentioning

confidence: 99%

“…Though not formally established (see Mushegian and Ebert, 2016 ), recent studies indicate a mutualistic relationship between formicine ants, and their gut-associated Acetobacteraceae ( Brown and Wernegreen, 2019 ; Chua et al, 2020 ). Thus, the creation of an acidic crop environment in formicine ants that is easier to endure if colonizing microbes are mutualists agrees with the concept of screening as a mechanism to choose microbial partners out of a pool of environmental microbes ( Archetti et al, 2011a ; Archetti et al, 2011b ; Biedermann and Kaltenpoth, 2014 ; Scheuring and Yu, 2012 ).…”

Section: Discussionmentioning

confidence: 99%

“…Apart from specialized intracellular endosymbionts associated with the midgut in the ant tribe Camponotini ( Degnan et al, 2004 ; Feldhaar et al, 2007 ; Russell et al, 2017 ; Williams and Wernegreen, 2015 ), formicine ant species have only low abundances of microbial associates in their gut lumen but carry members of the bacterial family Acetobacteraceae as a recurring part of their gut microbiota ( Brown and Wernegreen, 2016 ; Chua et al, 2018 ; He et al, 2011 ; Ivens et al, 2018 ; Russell et al, 2017 ). Some formicine gut-associated Acetobacteraceae show signs of genomic and metabolic adaptations to their host environment indicating coevolution and mutual benefit ( Brown and Wernegreen, 2019 ; Chua et al, 2020 ). But the recurrent presence of Acetobacteraceae in the gut of formicine ants potentially also reflects the direct transmission of bacteria among individuals, selective uptake on the part of the ants, specific adaptations for colonizing ant guts on the part of the bacteria, or some combination of all three ( Engel and Moran, 2013 ).…”

Section: Introductionmentioning

confidence: 99%

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

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Herrmann

Häfner

et al. 2020

eLife

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Animals continuously encounter microorganisms that are essential for health or cause disease. They are thus challenged to control harmful microbes while allowing the acquisition of beneficial microbes. This challenge is likely especially important for social insects with respect to microbes in food, as they often store food and exchange food among colony members. Here we show that formicine ants actively swallow their antimicrobial, highly acidic poison gland secretion. The ensuing acidic environment in the stomach, the crop, can limit the establishment of pathogenic and opportunistic microbes ingested with food and improve the survival of ants when faced with pathogen contaminated food. At the same time, crop acidity selectively allows acquisition and colonization by Acetobacteraceae, known bacterial gut associates of formicine ants. This suggests that swallowing of the poison in formicine ants acts as a microbial filter and that antimicrobials have a potentially widespread but so far underappreciated dual role in host-microbe interactions.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Tragust

Herrmann

Häfner

et al. 2020

eLife

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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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Oecophyllibacter saccharovoransgen. nov. sp. nov., a bacterial symbiont of the weaver antOecophylla smaragdina

Cited by 2 publications

References 71 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

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

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