6
views
0
recommends
+1 Recommend
1 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      How Hosts Taxonomy, Trophy, and Endosymbionts Shape Microbiome Diversity in Beetles

      research-article

      Read this article at

      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Bacterial communities play a crucial role in the biology, ecology, and evolution of multicellular organisms. In this research, the microbiome of 24 selected beetle species representing five families (Carabidae, Staphylinidae, Curculionidae, Chrysomelidae, Scarabaeidae) and three trophic guilds (carnivorous, herbivorous, detrivorous) was examined using 16S rDNA sequencing on the Illumina platform. The aim of the study was to compare diversity within and among species on various levels of organization, including evaluation of the impact of endosymbiotic bacteria. Collected data showed that beetles possess various bacterial communities and that microbiota of individuals of particular species hosts are intermixed. The most diverse microbiota were found in Carabidae and Scarabaeidae; the least diverse, in Staphylinidae. On higher organization levels, the diversity of bacteria was more dissimilar between families, while the most distinct with respect to their microbiomes were trophic guilds. Moreover, eight taxa of endosymbiotic bacteria were detected including common genera such as Wolbachia, Rickettsia, and Spiroplasma, as well as the rarely detected Cardinium, Arsenophonus, Buchnera, Sulcia, Regiella, and Serratia. There were no correlations among the abundance of the most common Wolbachia and Rickettsia; a finding that does not support the hypothesis that these bacteria occur interchangeably. The abundance of endosymbionts only weakly and negatively correlates with diversity of the whole microbiome in beetles. Overall, microbiome diversity was found to be more dependent on host phylogeny than on the abundance of endosymbionts. This is the first study in which bacteria diversity is compared between numerous species of beetles in a standardized manner.

          Electronic supplementary material

          The online version of this article (10.1007/s00248-019-01358-y) contains supplementary material, which is available to authorized users.

          Related collections

          Most cited references47

          • Record: found
          • Abstract: found
          • Article: not found

          Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling.

          The symbiotic microbiota profoundly affect many aspects of host physiology; however, the molecular mechanisms underlying host-microbe cross-talk are largely unknown. Here, we show that the pyrroloquinoline quinone-dependent alcohol dehydrogenase (PQQ-ADH) activity of a commensal bacterium, Acetobacter pomorum, modulates insulin/insulin-like growth factor signaling (IIS) in Drosophila to regulate host homeostatic programs controlling developmental rate, body size, energy metabolism, and intestinal stem cell activity. Germ-free animals monoassociated with PQQ-ADH mutant bacteria displayed severe deregulation of developmental and metabolic homeostasis. Importantly, these defects were reversed by enhancing host IIS or by supplementing the diet with acetic acid, the metabolic product of PQQ-ADH.
            Bookmark
            • Record: found
            • Abstract: found
            • Article: not found

            Wolbachia as a bacteriocyte-associated nutritional mutualist.

            Many insects are dependent on bacterial symbionts that provide essential nutrients (ex. aphid-Buchnera and tsetse-Wiglesworthia associations), wherein the symbionts are harbored in specific cells called bacteriocytes that constitute a symbiotic organ bacteriome. Facultative and parasitic bacterial symbionts like Wolbachia have been regarded as evolutionarily distinct from such obligate nutritional mutualists. However, we discovered that, in the bedbug Cimex lectularius, Wolbachia resides in a bacteriome and appears to be an obligate nutritional mutualist. Two bacterial symbionts, a Wolbachia strain and an unnamed gamma-proteobacterium, were identified from different strains of the bedbug. The Wolbachia symbiont was detected from all of the insects examined whereas the gamma-proteobacterium was found in a part of them. The Wolbachia symbiont was specifically localized in the bacteriomes and vertically transmitted via the somatic stem cell niche of germalia to oocytes, infecting the incipient symbiotic organ at an early stage of the embryogenesis. Elimination of the Wolbachia symbiont resulted in retarded growth and sterility of the host insect. These deficiencies were rescued by oral supplementation of B vitamins, confirming the essential nutritional role of the symbiont for the host. The estimated genome size of the Wolbachia symbiont was around 1.3 Mb, which was almost equivalent to the genome sizes of parasitic Wolbachia strains of other insects. These results indicate that bacteriocyte-associated nutritional mutualism can evolve from facultative and prevalent microbial associates like Wolbachia, highlighting a previously unknown aspect of the parasitism-mutualism evolutionary continuum.
              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              Multilocus sequence typing system for the endosymbiont Wolbachia pipientis.

              The eubacterial genus Wolbachia comprises one of the most abundant groups of obligate intracellular bacteria, and it has a host range that spans the phyla Arthropoda and Nematoda. Here we developed a multilocus sequence typing (MLST) scheme as a universal genotyping tool for Wolbachia. Internal fragments of five ubiquitous genes (gatB, coxA, hcpA, fbpA, and ftsZ) were chosen, and primers that amplified across the major Wolbachia supergroups found in arthropods, as well as other divergent lineages, were designed. A supplemental typing system using the hypervariable regions of the Wolbachia surface protein (WSP) was also developed. Thirty-seven strains belonging to supergroups A, B, D, and F obtained from singly infected hosts were characterized by using MLST and WSP. The number of alleles per MLST locus ranged from 25 to 31, and the average levels of genetic diversity among alleles were 6.5% to 9.2%. A total of 35 unique allelic profiles were found. The results confirmed that there is a high level of recombination in chromosomal genes. MLST was shown to be effective for detecting diversity among strains within a single host species, as well as for identifying closely related strains found in different arthropod hosts. Identical or similar allelic profiles were obtained for strains harbored by different insect species and causing distinct reproductive phenotypes. Strains with similar WSP sequences can have very different MLST allelic profiles and vice versa, indicating the importance of the MLST approach for strain identification. The MLST system provides a universal and unambiguous tool for strain typing, population genetics, and molecular evolutionary studies. The central database for storing and organizing Wolbachia bacterial and host information can be accessed at http://pubmlst.org/wolbachia/.
                Bookmark

                Author and article information

                Contributors
                +48 664404716 , michal.r.kolasa@gmail.com
                Journal
                Microb Ecol
                Microb. Ecol
                Microbial Ecology
                Springer US (New York )
                0095-3628
                1432-184X
                27 March 2019
                27 March 2019
                2019
                : 78
                : 4
                : 995-1013
                Affiliations
                [1 ]GRID grid.413454.3, ISNI 0000 0001 1958 0162, Institute of Systematics and Evolution of Animals, , Polish Academy of Sciences, ; Krakow, Poland
                [2 ]GRID grid.411201.7, ISNI 0000 0000 8816 7059, Department of Zoology and Animal Ecology, , University of Life Sciences in Lublin, ; Lublin, Poland
                [3 ]GRID grid.107891.6, ISNI 0000 0001 1010 7301, Institute of Biology, , University of Opole, ; Opole, Poland
                [4 ]GRID grid.5522.0, ISNI 0000 0001 2162 9631, Molecular and Behavioral Ecology Group, , Jagiellonian University, ; Krakow, Poland
                Author information
                http://orcid.org/0000-0003-2143-429X
                Article
                1358
                10.1007/s00248-019-01358-y
                6842344
                30915518
                b939dde5-c082-408a-81ef-14d91283c5cc
                © The Author(s) 2019

                Open Access This 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.

                History
                : 19 December 2018
                : 7 March 2019
                Funding
                Funded by: National Science Centre, Poland
                Award ID: DEC-2013/11/D/NZ8/00583
                Award Recipient :
                Funded by: Polish Ministry of Science and Higher Education
                Award ID: small grants for young researchers
                Categories
                Host Microbe Interactions
                Custom metadata
                © Springer Science+Business Media, LLC, part of Springer Nature 2019

                Microbiology & Virology
                bacterial community,host–microbe interactions,coleoptera,endosymbionts,microbial ecology

                Comments

                Comment on this article