Microbial composition of spiny ants (Hymenoptera: Formicidae: Polyrhachis) across their geographic range

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Abstract

Background

Symbiotic relationships between insects and bacteria are found across almost all insect orders, including Hymenoptera. However there are still many remaining questions about these associations including what factors drive host-associated bacterial composition. To better understand the evolutionary significance of this association in nature, further studies addressing a diversity of hosts across locations and evolutionary history are necessary. Ants of the genus Polyrhachis (spiny ants) are distributed across the Old World and exhibit generalist diets and habits. Using Next Generation Sequencing (NGS) and bioinformatics tools, this study explores the microbial community of >80 species of Polyrhachis distributed across the Old World and compares the microbiota of samples and related hosts across different biogeographic locations and in the context of their phylogenetic history.

Results

The predominant bacteria across samples were Enterobacteriaceae ( Blochmannia - with likely many new strains), followed by Wolbachia (with multiple strains), Lactobacillus, Thiotrichaceae, Acinetobacter, Nocardia, Sodalis, and others . We recovered some exclusive strains of Enterobacteriaceae as specific to some subgenera of Polyrhachis, corroborating the idea of coevolution between host and bacteria for this bacterial group. Our correlation results (partial mantel and mantel tests) found that host phylogeny can influence the overall bacterial community, but that geographic location had no effect.

Conclusions

Our work is revealing important aspects of the biology of hosts in structuring the diversity and abundance of these host-associated bacterial communities including the role of host phylogeny and shared evolutionary history.

Electronic supplementary material

The online version of this article (doi:10.1186/s12862-017-0945-8) contains supplementary material, which is available to authorized users.

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Most cited references 49

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The gut bacteria of insects: nonpathogenic interactions.

R. Dillon, V. Dillon (2004)

The diversity of the Insecta is reflected in the large and varied microbial communities inhabiting the gut. Studies, particularly with termites and cockroaches, have focused on the nutritional contributions of gut bacteria in insects living on suboptimal diets. The indigenous gut bacteria, however, also play a role in withstanding the colonization of the gut by non-indigenous species including pathogens. Gut bacterial consortia adapt by the transfer of plasmids and transconjugation between bacterial strains, and some insect species provide ideal conditions for bacterial conjugation, which suggests that the gut is a "hot spot" for gene transfer. Genomic analysis provides new avenues for the study of the gut microbial community and will reveal the molecular foundations of the relationships between the insect and its microbiome. In this review the intestinal bacteria is discussed in the context of developing our understanding of symbiotic relationships, of multitrophic interactions between insects and plant or animal host, and in developing new strategies for controlling insect pests.

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Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences

Jai Rideout, Yan-Yan He, Jose A. Navas-Molina … (2014)

We present a performance-optimized algorithm, subsampled open-reference OTU picking, for assigning marker gene (e.g., 16S rRNA) sequences generated on next-generation sequencing platforms to operational taxonomic units (OTUs) for microbial community analysis. This algorithm provides benefits over de novo OTU picking (clustering can be performed largely in parallel, reducing runtime) and closed-reference OTU picking (all reads are clustered, not only those that match a reference database sequence with high similarity). Because more of our algorithm can be run in parallel relative to “classic” open-reference OTU picking, it makes open-reference OTU picking tractable on massive amplicon sequence data sets (though on smaller data sets, “classic” open-reference OTU clustering is often faster). We illustrate that here by applying it to the first 15,000 samples sequenced for the Earth Microbiome Project (1.3 billion V4 16S rRNA amplicons). To the best of our knowledge, this is the largest OTU picking run ever performed, and we estimate that our new algorithm runs in less than 1/5 the time than would be required of “classic” open reference OTU picking. We show that subsampled open-reference OTU picking yields results that are highly correlated with those generated by “classic” open-reference OTU picking through comparisons on three well-studied datasets. An implementation of this algorithm is provided in the popular QIIME software package, which uses uclust for read clustering. All analyses were performed using QIIME’s uclust wrappers, though we provide details (aided by the open-source code in our GitHub repository) that will allow implementation of subsampled open-reference OTU picking independently of QIIME (e.g., in a compiled programming language, where runtimes should be further reduced). Our analyses should generalize to other implementations of these OTU picking algorithms. Finally, we present a comparison of parameter settings in QIIME’s OTU picking workflows and make recommendations on settings for these free parameters to optimize runtime without reducing the quality of the results. These optimized parameters can vastly decrease the runtime of uclust-based OTU picking in QIIME.

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Distinctive Gut Microbiota of Honey Bees Assessed Using Deep Sampling from Individual Worker Bees

Nancy Moran, Allison Hansen, J. Elijah Powell … (2012)

Surveys of 16S rDNA sequences from the honey bee, Apis mellifera, have revealed the presence of eight distinctive bacterial phylotypes in intestinal tracts of adult worker bees. Because previous studies have been limited to relatively few sequences from samples pooled from multiple hosts, the extent of variation in this microbiota among individuals within and between colonies and locations has been unclear. We surveyed the gut microbiota of 40 individual workers from two sites, Arizona and Maryland USA, sampling four colonies per site. Universal primers were used to amplify regions of 16S ribosomal RNA genes, and amplicons were sequenced using 454 pyrotag methods, enabling analysis of about 330,000 bacterial reads. Over 99% of these sequences belonged to clusters for which the first blastn hits in GenBank were members of the known bee phylotypes. Four phylotypes, one within Gammaproteobacteria (corresponding to “Candidatus Gilliamella apicola”) one within Betaproteobacteria (“Candidatus Snodgrassella alvi”), and two within Lactobacillus, were present in every bee, though their frequencies varied. The same typical bacterial phylotypes were present in all colonies and at both sites. Community profiles differed significantly among colonies and between sites, mostly due to the presence in some Arizona colonies of two species of Enterobacteriaceae not retrieved previously from bees. Analysis of Sanger sequences of rRNA of the Snodgrassella and Gilliamella phylotypes revealed that single bees contain numerous distinct strains of each phylotype. Strains showed some differentiation between localities, especially for the Snodgrassella phylotype.

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Author and article information

Contributors

Manuela Oliveira Ramalho:

ORCID: http://orcid.org/0000-0002-8144-6172

55 19 991220241 , manuramalho2010@gmail.com

Odair Correa Bueno: odaircb@rc.unesp.br

Corrie Saux Moreau: cmoreau@fieldmuseum.org

Journal

Journal ID (nlm-ta): BMC Evol Biol

Journal ID (iso-abbrev): BMC Evol. Biol

Title: BMC Evolutionary Biology

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2148

Publication date (Electronic): 5 April 2017

Publication date PMC-release: 5 April 2017

Publication date Collection: 2017

Volume: 17

Electronic Location Identifier: 96

Affiliations

[1 ]Universidade Estadual Paulista “Júlio de Mesquita Filho” UNESP – Campus Rio Claro, Biologia, CEIS. Av. 24A, 1515, Bela Vista, Rio Claro, SP 13506-900 Brazil

[2 ]Field Museum of Natural History, Department of Science and Education, Integrative Research Center, 1400 South Lake Shore Drive, Chicago, IL 60605 USA

Author information

Manuela Oliveira Ramalho http://orcid.org/0000-0002-8144-6172

Article

Publisher ID: 945

DOI: 10.1186/s12862-017-0945-8

PMC ID: 5382451

PubMed ID: 28381207

SO-VID: f41dd2cf-9491-47d5-8501-8d68a3859805

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 21 November 2016

Date accepted : 23 March 2017

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100006363, National Geographic Society;

Award ID: 9451-14

Award Recipient : Corrie Saux Moreau

Funded by: CAPES Foundation

Award ID: 007343/2014-00

Award Recipient : Manuela Oliveira Ramalho

Custom metadata

ScienceOpen disciplines: Evolutionary Biology

Keywords: blochmannia,wolbachia,lactobacillus,ngs,microbes,amplicon sequencing

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ScienceOpen disciplines: Evolutionary Biology

Keywords: blochmannia, wolbachia, lactobacillus, ngs, microbes, amplicon sequencing

Microbial composition of spiny ants (Hymenoptera: Formicidae: Polyrhachis) across their geographic range

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Hymenoptera

Most cited references 49

The gut bacteria of insects: nonpathogenic interactions.

Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences

Distinctive Gut Microbiota of Honey Bees Assessed Using Deep Sampling from Individual Worker Bees

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