TY - JOUR
T1 - A bacterial filter protects and structures the gut microbiome of an insect
AU - Lanan, Michele Caroline
AU - Rodrigues, Pedro Augusto Pos
AU - Agellon, Al
AU - Jansma, Patricia
AU - Wheeler, Diana Esther
N1 - Funding Information:
We wish to thank Wulfila Gronenberg, Mike Riehle, Tony Day, Gina Zhang and Joe Cicero for assistance in learning techniques. We also thank Nick Waser, Peter Waser, Andrew Waser, Mary Price, Judith Bronstein, Amity Wilczek, Gordon Snelling, Corinne Stouthamer and Terry McGlynn for comments on previous drafts of the manuscript. This work was funded by NIH grant 5K12GM000708-13. PAPR received support from NSF Grant 0604067 to DEW.
Publisher Copyright:
© 2016 International Society for Microbial Ecology All rights reserved.
PY - 2016/8/1
Y1 - 2016/8/1
N2 - Associations with symbionts within the gut lumen of hosts are particularly prone to disruption due to the constant influx of ingested food and non-symbiotic microbes, yet we know little about how partner fidelity is maintained. Here we describe for the first time the existence of a gut morphological filter capable of protecting an animal gut microbiome from disruption. The proventriculus, a valve located between the crop and midgut of insects, functions as a micro-pore filter in the Sonoran Desert turtle ant (Cephalotes rohweri), blocking the entry of bacteria and particles ≥0.2 μm into the midgut and hindgut while allowing passage of dissolved nutrients. Initial establishment of symbiotic gut bacteria occurs within the first few hours after pupation via oral-rectal trophallaxis, before the proventricular filter develops. Cephalotes ants are remarkable for having maintained a consistent core gut microbiome over evolutionary time and this partner fidelity is likely enabled by the proventricular filtering mechanism. In addition, the structure and function of the cephalotine proventriculus offers a new perspective on organismal resistance to pathogenic microbes, structuring of gut microbial communities, and development and maintenance of host-microbe fidelity both during the animal life cycle and over evolutionary time.
AB - Associations with symbionts within the gut lumen of hosts are particularly prone to disruption due to the constant influx of ingested food and non-symbiotic microbes, yet we know little about how partner fidelity is maintained. Here we describe for the first time the existence of a gut morphological filter capable of protecting an animal gut microbiome from disruption. The proventriculus, a valve located between the crop and midgut of insects, functions as a micro-pore filter in the Sonoran Desert turtle ant (Cephalotes rohweri), blocking the entry of bacteria and particles ≥0.2 μm into the midgut and hindgut while allowing passage of dissolved nutrients. Initial establishment of symbiotic gut bacteria occurs within the first few hours after pupation via oral-rectal trophallaxis, before the proventricular filter develops. Cephalotes ants are remarkable for having maintained a consistent core gut microbiome over evolutionary time and this partner fidelity is likely enabled by the proventricular filtering mechanism. In addition, the structure and function of the cephalotine proventriculus offers a new perspective on organismal resistance to pathogenic microbes, structuring of gut microbial communities, and development and maintenance of host-microbe fidelity both during the animal life cycle and over evolutionary time.
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U2 - 10.1038/ismej.2015.264
DO - 10.1038/ismej.2015.264
M3 - Article
C2 - 26872040
AN - SCOPUS:84957894957
SN - 1751-7362
VL - 10
SP - 1866
EP - 1876
JO - ISME Journal
JF - ISME Journal
IS - 8
ER -