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      Symbionts as Major Modulators of Insect Health: Lactic Acid Bacteria and Honeybees

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          Abstract

          Lactic acid bacteria (LAB) are well recognized beneficial host-associated members of the microbiota of humans and animals. Yet LAB-associations of invertebrates have been poorly characterized and their functions remain obscure. Here we show that honeybees possess an abundant, diverse and ancient LAB microbiota in their honey crop with beneficial effects for bee health, defending them against microbial threats. Our studies of LAB in all extant honeybee species plus related apid bees reveal one of the largest collections of novel species from the genera Lactobacillus and Bifidobacterium ever discovered within a single insect and suggest a long (>80 mya) history of association. Bee associated microbiotas highlight Lactobacillus kunkeei as the dominant LAB member. Those showing potent antimicrobial properties are acquired by callow honey bee workers from nestmates and maintained within the crop in biofilms, though beekeeping management practices can negatively impact this microbiota. Prophylactic practices that enhance LAB, or supplementary feeding of LAB, may serve in integrated approaches to sustainable pollinator service provision. We anticipate this microbiota will become central to studies on honeybee health, including colony collapse disorder, and act as an exemplar case of insect-microbe symbiosis.

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          Most cited references 49

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          The gut bacteria of insects: nonpathogenic interactions.

          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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            Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens.

            The gastrointestinal tract is a complex ecosystem that associates a resident microbiota and cells of various phenotypes lining the epithelial wall expressing complex metabolic activities. The resident microbiota in the digestive tract is a heterogeneous microbial ecosystem containing up to 1 x 10(14) colony-forming units (CFUs) of bacteria. The intestinal microbiota plays an important role in normal gut function and maintaining host health. The host is protected from attack by potentially harmful microbial microorganisms by the physical and chemical barriers created by the gastrointestinal epithelium. The cells lining the gastrointestinal epithelium and the resident microbiota are two partners that properly and/or synergistically function to promote an efficient host system of defence. The gastrointestinal cells that make up the epithelium, provide a physical barrier that protects the host against the unwanted intrusion of microorganisms into the gastrointestinal microbiota, and against the penetration of harmful microorganisms which usurp the cellular molecules and signalling pathways of the host to become pathogenic. One of the basic physiological functions of the resident microbiota is that it functions as a microbial barrier against microbial pathogens. The mechanisms by which the species of the microbiota exert this barrier effect remain largely to be determined. There is increasing evidence that lactobacilli and bifidobacteria, which inhabit the gastrointestinal microbiota, develop antimicrobial activities that participate in the host's gastrointestinal system of defence. The objective of this review is to analyze the in vitro and in vivo experimental and clinical studies in which the antimicrobial activities of selected lactobacilli and bifidobacteria strains have been documented.
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              Diversity of the human gastrointestinal tract microbiota revisited.

              Since the early days of microbiology, more than a century ago, representatives of over 400 different microbial species have been isolated and fully characterized from human gastrointestinal samples. However, during the past decade molecular ecological studies based on ribosomal RNA (rRNA) sequences have revealed that cultivation has been able only to access a small fraction of the microbial diversity within the gastrointestinal tract. The increasing number of deposited rRNA sequences calls for the setting up a curated database that allows handling of the excessive degree of redundancy that threatens the usability of public databases. The integration of data from cultivation-based studies and molecular inventories of small subunit (SSU) rRNA diversity, presented here for the first time, provides a systematic framework of the microbial diversity in the human gastrointestinal tract of more than 1000 different species-level phylogenetic types (phylotypes). Such knowledge is essential for the design of high-throughput approaches such as phylogenetic DNA microarrays for the comprehensive analysis of gastrointestinal tract microbiota at multiple levels of taxonomic resolution. Development of such approaches is likely to be pivotal to generating novel insights in microbiota functionality in health and disease.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2012
                12 March 2012
                : 7
                : 3
                Affiliations
                [1 ]Department of Laboratory Medicine, Medical Microbiology, Lund University, Lund, Sweden
                [2 ]Department of Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden
                [3 ]School of Biological Sciences, Queen's University Belfast, Belfast, United Kingdom
                [4 ]Institute for Biology, Martin-Luther-University Halle-Wittenberg, Halle (Saale), Germany
                [5 ]Department of Microbiology, Tumor and Cell Biology (MTC), Karolinska Institutet, Stockholm, Sweden
                University of Hyderabad, India
                Author notes

                Conceived and designed the experiments: TCO AV. Performed the experiments: TCO AV IF E. Forsgren E. Flaberg LS. Analyzed the data: AV TCO E. Forsgren IF RJP E. Flaberg LS. Contributed reagents/materials/analysis tools: RJP. Wrote the paper: AV RJP TCO.

                Article
                PONE-D-12-02065
                10.1371/journal.pone.0033188
                3299755
                22427985
                Vásquez et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                Page count
                Pages: 9
                Categories
                Research Article
                Agriculture
                Agricultural Production
                Biology
                Ecology
                Agroecology
                Community Ecology
                Microbiology
                Bacteriology
                Zoology

                Uncategorized

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