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      Recent infection by Wolbachia alters microbial communities in wild Laodelphax striatellus populations

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          Abstract

          Background

          Host-associated microbial communities play an important role in the fitness of insect hosts. However, the factors shaping microbial communities in wild populations, including genetic background, ecological factors, and interactions among microbial species, remain largely unknown.

          Results

          Here, we surveyed microbial communities of the small brown planthopper (SBPH, Laodelphax striatellus) across 17 geographical populations in China and Japan by using 16S rRNA amplicon sequencing. Using structural equation models (SEM) and Mantel analyses, we show that variation in microbial community structure is likely associated with longitude, annual mean precipitation (Bio12), and mitochondrial DNA variation. However, a Wolbachia infection, which is spreading to northern populations of SBPH, seems to have a relatively greater role than abiotic factors in shaping microbial community structure, leading to sharp decreases in bacterial taxon diversity and abundance in host-associated microbial communities. Comparative RNA-Seq analyses between Wolbachia-infected and -uninfected strains indicate that the Wolbachia do not seem to alter the immune reaction of SBPH, although Wolbachia affected expression of metabolism genes.

          Conclusion

          Together, our results identify potential factors and interactions among different microbial species in the microbial communities of SBPH, which can have effects on insect physiology, ecology, and evolution.

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          Most cited references42

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          FLASH: fast length adjustment of short reads to improve genome assemblies.

          Next-generation sequencing technologies generate very large numbers of short reads. Even with very deep genome coverage, short read lengths cause problems in de novo assemblies. The use of paired-end libraries with a fragment size shorter than twice the read length provides an opportunity to generate much longer reads by overlapping and merging read pairs before assembling a genome. We present FLASH, a fast computational tool to extend the length of short reads by overlapping paired-end reads from fragment libraries that are sufficiently short. We tested the correctness of the tool on one million simulated read pairs, and we then applied it as a pre-processor for genome assemblies of Illumina reads from the bacterium Staphylococcus aureus and human chromosome 14. FLASH correctly extended and merged reads >99% of the time on simulated reads with an error rate of <1%. With adequately set parameters, FLASH correctly merged reads over 90% of the time even when the reads contained up to 5% errors. When FLASH was used to extend reads prior to assembly, the resulting assemblies had substantially greater N50 lengths for both contigs and scaffolds. The FLASH system is implemented in C and is freely available as open-source code at http://www.cbcb.umd.edu/software/flash. t.magoc@gmail.com.
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            Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera.

            A Douglas (1998)
            Most aphids possess intracellular bacteria of the genus Buchnera. The bacteria are transmitted vertically via the aphid ovary, and the association is obligate for both partners: Bacteria-free aphids grow poorly and produce few or no offspring, and Buchnera are both unknown apart from aphids and apparently unculturable. The symbiosis has a nutritional basis. Specifically, bacterial provisioning of essential amino acids has been demonstrated. Nitrogen recycling, however, is not quantitatively important to the nutrition of aphid species studied, and there is strong evidence against bacterial involvement in the lipid and sterol nutrition of aphids. Buchnera have been implicated in various non-nutritional functions. Of these, just one has strong experimental support: promotion of aphid transmission of circulative viruses. It is argued that strong parallels may exist between the nutritional interactions (including the underlying mechanisms) in the aphid-Buchnera association and other insect symbioses with intracellular microorganisms.
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              Mosquitoes rely on their gut microbiota for development.

              Field studies indicate adult mosquitoes (Culicidae) host low diversity communities of bacteria that vary greatly among individuals and species. In contrast, it remains unclear how adult mosquitoes acquire their microbiome, what influences community structure, and whether the microbiome is important for survival. Here, we used pyrosequencing of 16S rRNA to characterize the bacterial communities of three mosquito species reared under identical conditions. Two of these species, Aedes aegypti and Anopheles gambiae, are anautogenous and must blood-feed to produce eggs, while one, Georgecraigius atropalpus, is autogenous and produces eggs without blood feeding. Each mosquito species contained a low diversity community comprised primarily of aerobic bacteria acquired from the aquatic habitat in which larvae developed. Our results suggested that the communities in Ae. aegypti and An. gambiae larvae share more similarities with one another than with G. atropalpus. Studies with Ae. aegypti also strongly suggested that adults transstadially acquired several members of the larval bacterial community, but only four genera of bacteria present in blood fed females were detected on eggs. Functional assays showed that axenic larvae of each species failed to develop beyond the first instar. Experiments with Ae. aegypti indicated several members of the microbial community and Escherichia coli successfully colonized axenic larvae and rescued development. Overall, our results provide new insights about the acquisition and structure of bacterial communities in mosquitoes. They also indicate that three mosquito species spanning the breadth of the Culicidae depend on their gut microbiome for development. © 2014 John Wiley & Sons Ltd.
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                Author and article information

                Contributors
                xyhong@njau.edu.cn
                Journal
                Microbiome
                Microbiome
                Microbiome
                BioMed Central (London )
                2049-2618
                2 July 2020
                2 July 2020
                2020
                : 8
                : 104
                Affiliations
                [1 ]GRID grid.27871.3b, ISNI 0000 0000 9750 7019, Department of Entomology, , Nanjing Agricultural University, ; Nanjing, 210095 Jiangsu China
                [2 ]GRID grid.482768.7, ISNI 0000 0001 0805 348X, NARO Kyushu Okinawa Agricultural Research Center, ; 2421 Suya, Koshi, Kumamoto, 861-1192 Japan
                [3 ]GRID grid.1008.9, ISNI 0000 0001 2179 088X, School of BioSciences, Bio21 Institute, , The University of Melbourne, ; Melbourne, Victoria 3010 Australia
                Author information
                http://orcid.org/0000-0002-5209-3961
                Article
                878
                10.1186/s40168-020-00878-x
                7333401
                32616041
                0c79b2cc-52b6-463a-8ebd-2651ee25de77
                © The Author(s) 2020

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.

                History
                : 3 May 2020
                : 1 June 2020
                Funding
                Funded by: National Natural Science Foundation of China
                Award ID: 31672035 and 31871976
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000925, National Health and Medical Research Council;
                Categories
                Research
                Custom metadata
                © The Author(s) 2020

                laodelphax striatellus,microbial community,wolbachia,endosymbiont,microbial interactions

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