Microbial Diversity in the Midguts of Field and Lab-Reared Populations of the European Corn Borer Ostrinia nubilalis

PLOS ONE, Jun 2011

Background Insects are associated with microorganisms that contribute to the digestion and processing of nutrients. The European Corn Borer (ECB) is a moth present world-wide, causing severe economical damage as a pest on corn and other crops. In the present work, we give a detailed view of the complexity of the microorganisms forming the ECB midgut microbiota with the objective of comparing the biodiversity of the midgut-associated microbiota and explore their potential as a source of genes and enzymes with biotechnological applications. Methodological/Principal Findings A high-throughput sequencing approach has been used to identify bacterial species, genes and metabolic pathways, particularly those involved in plant-matter degradation, in two different ECB populations (field-collected vs. lab-reared population with artificial diet). Analysis of the resulting sequences revealed the massive presence of Staphylococcus warneri and Weissella paramesenteroides in the lab-reared sample. This enabled us to reconstruct both genomes almost completely. Despite the apparently low diversity, 208 different genera were detected in the sample, although most of them at very low frequency. By contrast, the natural population exhibited an even higher taxonomic diversity along with a wider array of cellulolytic enzyme families. However, in spite of the differences in relative abundance of major taxonomic groups, not only did both metagenomes share a similar functional profile but also a similar distribution of non-redundant genes in different functional categories. Conclusions/Significance Our results reveal a highly diverse pool of bacterial species in both O. nubilalis populations, with major differences: The lab-reared sample is rich in gram-positive species (two of which have almost fully sequenced genomes) while the field sample harbors mainly gram-negative species and has a larger set of cellulolytic enzymes. We have found a clear relationship between the diet and the midgut microbiota, which reveals the selection pressure of food on the community of intestinal bacteria.

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Microbial Diversity in the Midguts of Field and Lab-Reared Populations of the European Corn Borer Ostrinia nubilalis

et al. (2011) Microbial Diversity in the Midguts of Field and Lab-Reared Populations of the European Corn Borer Ostrinia nubilalis. PLoS ONE 6(6): e21751. doi:10.1371/journal.pone.0021751 Microbial Diversity in the Midguts of Field and Lab-Reared Populations of the European Corn Borer Ostrinia nubilalis Eugeni Belda 0 Laia Pedrola 0 Juli Pereto 0 Juan F. Martnez-Blanch 0 Arnau Montagud 0 Emilio 0 Navarro 0 Javier Urchuegua 0 Daniel Ramo n 0 Andre s Moya 0 Manuel Porcar 0 Purification Lopez-Garcia, Universite Paris Sud, France 0 1 Institut Cavanilles de Biodiversitat i Biologia Evolutiva, University of Valencia , Valencia , Spain , 2 Instituto Universitario de Matema tica Pura y Aplicada, Universitat Polite`cnica de Vale`ncia , Valencia, Spain, 3 Lifesequencing, Valencia , Spain , 4 Departamento de Lenguajes y Ciencias de la Computacio n, Campus de Teatinos, Universidad de Ma laga , Ma laga , Spain Background: Insects are associated with microorganisms that contribute to the digestion and processing of nutrients. The European Corn Borer (ECB) is a moth present world-wide, causing severe economical damage as a pest on corn and other crops. In the present work, we give a detailed view of the complexity of the microorganisms forming the ECB midgut microbiota with the objective of comparing the biodiversity of the midgut-associated microbiota and explore their potential as a source of genes and enzymes with biotechnological applications. Methodological/Principal Findings: A high-throughput sequencing approach has been used to identify bacterial species, genes and metabolic pathways, particularly those involved in plant-matter degradation, in two different ECB populations (field-collected vs. lab-reared population with artificial diet). Analysis of the resulting sequences revealed the massive presence of Staphylococcus warneri and Weissella paramesenteroides in the lab-reared sample. This enabled us to reconstruct both genomes almost completely. Despite the apparently low diversity, 208 different genera were detected in the sample, although most of them at very low frequency. By contrast, the natural population exhibited an even higher taxonomic diversity along with a wider array of cellulolytic enzyme families. However, in spite of the differences in relative abundance of major taxonomic groups, not only did both metagenomes share a similar functional profile but also a similar distribution of non-redundant genes in different functional categories. Conclusions/Significance: Our results reveal a highly diverse pool of bacterial species in both O. nubilalis populations, with major differences: The lab-reared sample is rich in gram-positive species (two of which have almost fully sequenced genomes) while the field sample harbors mainly gram-negative species and has a larger set of cellulolytic enzymes. We have found a clear relationship between the diet and the midgut microbiota, which reveals the selection pressure of food on the community of intestinal bacteria. Current address; CEA-GENOSCOPE; Laboratorie d'Analyse Bioinformatique en Geno mique et Metabolisme; Evry; France - Funding: The research was funded by the Spanish Ministerio de Ciencia e Innovacio n, under grant agreement CIT-010000-2008-5 and by a MICINN (Ministerio de Ciencia e Innovacio n) TIN2009-12359 ArtBioCom project. Arnau Montagud acknowledges Generalitat Valenciana grant BFPI/2007/283. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: Daniel Ramo n, Juan F. Martnez and Laia Pedrola are employed by a commercial company: Lifesequencing (Valencia, Spain). This does not alter the authors adherence to all the PLoS ONE policies on sharing data and materials. All the authors have declared that no competing interests (financial or non-financial, professional, or personal) exist. Insects and related arthropods are a source of molecules of biotechnological interest, from the high-performing silk of spiders and silkworms, which is mimicked in the so-called bioinspired materials [1], to cellulolytic enzymes for biofuel production or paper waste treatment. Additionally, insect-associated microorganisms, particularly endosymbionts, are known to produce bioactive compounds that protect the host against adverse environmental conditions, predators or competitors and they have thus been suggested as suitable for biotechnological applications [2]. Most insects are phytophagous, and they harbor a microbiota specialized in the hydrolysis and fermentation of plant biomass in their guts. An obvious biotechnological application of this ecosystem lies in the identification and characterization of target molecules involved in lignocellulosic degradation, by way of next-generation sequencing technologies [3]. Metagenomics is a powerful tool that can reveal the genomic diversity of natural environments but, up to date, only a few reports exist on metagenomics of insec (...truncated)


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Eugeni Belda, Laia Pedrola, Juli Peretó, Juan F. Martínez-Blanch, Arnau Montagud, Emilio Navarro, Javier Urchueguía, Daniel Ramón, Andrés Moya, Manuel Porcar. Microbial Diversity in the Midguts of Field and Lab-Reared Populations of the European Corn Borer Ostrinia nubilalis, PLOS ONE, 2011, Volume 6, Issue 6, DOI: 10.1371/journal.pone.0021751