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Open Access Research article

A unique midgut-associated bacterial community hosted by the cave beetle Cansiliella servadeii (Coleoptera: Leptodirini) reveals parallel phylogenetic divergences from universal gut-specific ancestors

Maurizio G Paoletti1, Luca Mazzon2, Isabel Martinez-Sañudo2, Mauro Simonato2, Mattia Beggio1, Angelo Leandro Dreon1, Alberto Pamio1, Mauro Brilli3, Luca Dorigo4, Annette Summers Engel5, Alessandra Tondello1, Barbara Baldan1, Giuseppe Concheri2 and Andrea Squartini2*

Author Affiliations

1 Dipartimento di Biologia, Università di Padova, via U. Bassi 58/B, Padova, 35131, Italy

2 Dipartimento di Agronomia Animali Alimenti Risorse Naturali e Ambiente, Università di Padova - Agripolis, Viale dell’Università, Padova, Legnaro, 16 - 35020, , Italy

3 Istituto di Geologia Ambientale e Geoingegneria, Dipartimento di Scienze della Terra, Università La Sapienza di Roma, Rome, 00185, Italy

4 Natural History Museum, Via Marangoni 39, Udine, 33100, Italy

5 Department of Earth and Planetary Sciences, University of Tennessee, Knoxville, TN, 37996,, USA

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BMC Microbiology 2013, 13:129  doi:10.1186/1471-2180-13-129

Published: 10 June 2013

Abstract

Background

Cansiliella servadeii (Coleoptera) is an endemic troglobite living in deep carbonate caves in North-Eastern Italy. The beetle constantly moves and browses in its preferred habitat (consisting in flowing water and moonmilk, a soft speleothem colonized by microorganisms) self-preens to convey material from elytra, legs, and antennae towards the mouth. We investigated its inner and outer microbiota using microscopy and DNA-based approaches.

Results

Abundant microbial cell masses were observed on the external appendages. Cansiliella’s midgut is fully colonized by live microbes and culture-independent analyses yielded nearly 30 different 16S phylotypes that have no overlap with the community composition of the moonmilk. Many of the lineages, dominated by Gram positive groups, share very low similarity to database sequences. However for most cases, notwithstanding their very limited relatedness with existing records, phylotypes could be assigned to bacterial clades that had been retrieved from insect or other animals’ digestive traits.

Conclusions

Results suggest a history of remote separation from a common ancestor that harboured a set of gut-specific bacteria whose functions are supposedly critical for host physiology. The phylogenetic and coevolutionary implications of the parallel occurrences of these prokaryotic guilds appear to apply throughout a broad spectrum of animal diversity. Their persistence and conservation underlies a possibly critical role of precise bacterial assemblages in animal-bacteria interactions.

Keywords:
Cansiliella servadeii; Gut bacteria; Animal-bacteria coevolution; Cave; Moonmilk; Food web