38
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      A bacterial filter protects and structures the gut microbiome of an insect

      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

          Associations with symbionts within the gut lumen of hosts are particularly prone to disruption due to the constant influx of ingested food and non-symbiotic microbes, yet we know little about how partner fidelity is maintained. Here we describe for the first time the existence of a gut morphological filter capable of protecting an animal gut microbiome from disruption. The proventriculus, a valve located between the crop and midgut of insects, functions as a micro-pore filter in the Sonoran Desert turtle ant ( Cephalotes rohweri), blocking the entry of bacteria and particles ⩾0.2 μm into the midgut and hindgut while allowing passage of dissolved nutrients. Initial establishment of symbiotic gut bacteria occurs within the first few hours after pupation via oral–rectal trophallaxis, before the proventricular filter develops. Cephalotes ants are remarkable for having maintained a consistent core gut microbiome over evolutionary time and this partner fidelity is likely enabled by the proventricular filtering mechanism. In addition, the structure and function of the cephalotine proventriculus offers a new perspective on organismal resistance to pathogenic microbes, structuring of gut microbial communities, and development and maintenance of host–microbe fidelity both during the animal life cycle and over evolutionary time.

          Related collections

          Most cited references26

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

          Molecular biology and pathogenicity of mycoplasmas.

          The recent sequencing of the entire genomes of Mycoplasma genitalium and M. pneumoniae has attracted considerable attention to the molecular biology of mycoplasmas, the smallest self-replicating organisms. It appears that we are now much closer to the goal of defining, in molecular terms, the entire machinery of a self-replicating cell. Comparative genomics based on comparison of the genomic makeup of mycoplasmal genomes with those of other bacteria, has opened new ways of looking at the evolutionary history of the mycoplasmas. There is now solid genetic support for the hypothesis that mycoplasmas have evolved as a branch of gram-positive bacteria by a process of reductive evolution. During this process, the mycoplasmas lost considerable portions of their ancestors' chromosomes but retained the genes essential for life. Thus, the mycoplasmal genomes carry a high percentage of conserved genes, greatly facilitating gene annotation. The significant genome compaction that occurred in mycoplasmas was made possible by adopting a parasitic mode of life. The supply of nutrients from their hosts apparently enabled mycoplasmas to lose, during evolution, the genes for many assimilative processes. During their evolution and adaptation to a parasitic mode of life, the mycoplasmas have developed various genetic systems providing a highly plastic set of variable surface proteins to evade the host immune system. The uniqueness of the mycoplasmal systems is manifested by the presence of highly mutable modules combined with an ability to expand the antigenic repertoire by generating structural alternatives, all compressed into limited genomic sequences. In the absence of a cell wall and a periplasmic space, the majority of surface variable antigens in mycoplasmas are lipoproteins. Apart from providing specific antimycoplasmal defense, the host immune system is also involved in the development of pathogenic lesions and exacerbation of mycoplasma induced diseases. Mycoplasmas are able to stimulate as well as suppress lymphocytes in a nonspecific, polyclonal manner, both in vitro and in vivo. As well as to affecting various subsets of lymphocytes, mycoplasmas and mycoplasma-derived cell components modulate the activities of monocytes/macrophages and NK cells and trigger the production of a wide variety of up-regulating and down-regulating cytokines and chemokines. Mycoplasma-mediated secretion of proinflammatory cytokines, such as tumor necrosis factor alpha, interleukin-1 (IL-1), and IL-6, by macrophages and of up-regulating cytokines by mitogenically stimulated lymphocytes plays a major role in mycoplasma-induced immune system modulation and inflammatory responses.
            Bookmark
            • Record: found
            • Abstract: found
            • Article: not found

            New insights into peritrophic matrix synthesis, architecture, and function.

            The peritrophic matrix (PM) is a chitin and glycoprotein layer that lines the invertebrate midgut. Although structurally different, it is functionally similar to the mucous secretions of the vertebrate digestive tract. The PM is a physical barrier, protecting the midgut epithelium from abrasive food particles, digestive enzymes, and pathogens infectious per os. It is also a biochemical barrier, sequestering and, in some cases, inactivating ingested toxins. Finally, the PM compartmentalizes digestive processes, allowing for efficient nutrient acquisition and reuse of hydrolytic enzymes. The PM consists of an organized lattice of chitin fibrils held together by chitin binding proteins. Glycans fill the interstitial spaces, creating a molecular sieve, the properties of which are dependent on the immediate ion content and pH. In this review, we have integrated recent structural and functional information to create a holistic model for the PM. We also show how this information may generate novel technologies for use in insect pest management.
              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants.

              Ants are a dominant feature of terrestrial ecosystems, yet we know little about the forces that drive their evolution. Recent findings illustrate that their diets range from herbivorous to predaceous, with "herbivores" feeding primarily on exudates from plants and sap-feeding insects. Persistence on these nitrogen-poor food sources raises the question of how ants obtain sufficient nutrition. To investigate the potential role of symbiotic microbes, we have surveyed 283 species from 18 of the 21 ant subfamilies using molecular techniques. Our findings uncovered a wealth of bacteria from across the ants. Notable among the surveyed hosts were herbivorous "turtle ants" from the related genera Cephalotes and Procryptocerus (tribe Cephalotini). These commonly harbored bacteria from ant-specific clades within the Burkholderiales, Pseudomonadales, Rhizobiales, Verrucomicrobiales, and Xanthomonadales, and studies of lab-reared Cephalotes varians characterized these microbes as symbiotic residents of ant guts. Although most of these symbionts were confined to turtle ants, bacteria from an ant-specific clade of Rhizobiales were more broadly distributed. Statistical analyses revealed a strong relationship between herbivory and the prevalence of Rhizobiales gut symbionts within ant genera. Furthermore, a consideration of the ant phylogeny identified at least five independent origins of symbioses between herbivorous ants and related Rhizobiales. Combined with previous findings and the potential for symbiotic nitrogen fixation, our results strongly support the hypothesis that bacteria have facilitated convergent evolution of herbivory across the ants, further implicating symbiosis as a major force in ant evolution.
                Bookmark

                Author and article information

                Journal
                ISME J
                ISME J
                The ISME Journal
                Nature Publishing Group
                1751-7362
                1751-7370
                August 2016
                12 February 2016
                1 August 2016
                : 10
                : 8
                : 1866-1876
                Affiliations
                [1 ]Chair of the Natural Sciences, Deep Springs College , Big Pine, CA, USA
                [2 ]Graduate Interdisciplinary Program in Entomology and Insect Science, University of Arizona , Tucson, AZ, USA
                [3 ]School of Animal and Comparative Biomedical Sciences, University of Arizona , Tucson, AZ, USA
                [4 ]Department of Neuroscience, University of Arizona , Tucson, AZ, USA
                [5 ]Department of Entomology, University of Arizona , Tucson, AZ, USA
                Author notes
                [* ]Chair of the Natural Sciences, Deep Springs College , Big Pine, CA 93513, USA. E-mail: lanan@ 123456deepsprings.edu
                [6]

                These two authors contributed equally to this work.

                Article
                ismej2015264
                10.1038/ismej.2015.264
                5029173
                26872040
                212915ee-cbad-400f-bf10-9d1d64db933b
                Copyright © 2016 International Society for Microbial Ecology

                This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/4.0/

                History
                : 04 October 2015
                : 02 December 2015
                : 14 December 2015
                Categories
                Original Article

                Microbiology & Virology
                Microbiology & Virology

                Comments

                Comment on this article