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      Unity Makes Strength: A Review on Mutualistic Symbiosis in Representative Insect Clades

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          Abstract

          Settled on the foundations laid by zoologists and embryologists more than a century ago, the study of symbiosis between prokaryotes and eukaryotes is an expanding field. In this review, we present several models of insect–bacteria symbioses that allow for the detangling of most known features of this distinctive way of living, using a combination of very diverse screening approaches, including molecular, microscopic, and genomic techniques. With the increasing the amount of endosymbiotic bacteria genomes available, it has been possible to develop evolutionary models explaining the changes undergone by these bacteria in their adaptation to the intracellular host environment. The establishment of a given symbiotic system can be a root cause of substantial changes in the partners’ way of life. Furthermore, symbiont replacement and/or the establishment of bacterial consortia are two ways in which the host can exploit its interaction with environmental bacteria for endosymbiotic reinvigoration. The detailed study of diverse and complex symbiotic systems has revealed a great variety of possible final genomic products, frequently below the limit considered compatible with cellular life, and sometimes with unanticipated genomic and population characteristics, raising new questions that need to be addressed in the near future through a wider exploration of new models and empirical observations.

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          Most cited references124

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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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            Learning how to live together: genomic insights into prokaryote-animal symbioses.

            Our understanding of prokaryote-eukaryote symbioses as a source of evolutionary innovation has been rapidly increased by the advent of genomics, which has made possible the biological study of uncultivable endosymbionts. Genomics is allowing the dissection of the evolutionary process that starts with host invasion then progresses from facultative to obligate symbiosis and ends with replacement by, or coexistence with, new symbionts. Moreover, genomics has provided important clues on the mechanisms driving the genome-reduction process, the functions that are retained by the endosymbionts, the role of the host, and the factors that might determine whether the association will become parasitic or mutualistic.
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              Determination of the core of a minimal bacterial gene set.

              The availability of a large number of complete genome sequences raises the question of how many genes are essential for cellular life. Trying to reconstruct the core of the protein-coding gene set for a hypothetical minimal bacterial cell, we have performed a computational comparative analysis of eight bacterial genomes. Six of the analyzed genomes are very small due to a dramatic genome size reduction process, while the other two, corresponding to free-living relatives, are larger. The available data from several systematic experimental approaches to define all the essential genes in some completely sequenced bacterial genomes were also considered, and a reconstruction of a minimal metabolic machinery necessary to sustain life was carried out. The proposed minimal genome contains 206 protein-coding genes with all the genetic information necessary for self-maintenance and reproduction in the presence of a full complement of essential nutrients and in the absence of environmental stress. The main features of such a minimal gene set, as well as the metabolic functions that must be present in the hypothetical minimal cell, are discussed.
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                Author and article information

                Journal
                Life (Basel)
                Life (Basel)
                life
                Life
                MDPI
                2075-1729
                25 February 2019
                March 2019
                : 9
                : 1
                : 21
                Affiliations
                [1 ]Institute for Integrative Systems Biology (I2SysBio), Universitat de València/CSIC. Calle Catedrático Agustín Escardino, 9, 46980 Paterna (Valencia), Spain
                [2 ]Departament de Genètica, Universitat de València. Calle Dr. Moliner, 50, 46100 Burjassot (València), Spain
                [3 ]Área de Genómica y Salud, Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunidad Valenciana (FISABIO). Avenida de Cataluña 21, 46020 València, Spain
                Author notes
                [* ]Correspondence: rosario.gil@ 123456uv.es (R.G.); amparo.latorre@ 123456uv.es (A.L.) Tel.: +34-96-354-3824 (R.G.); +34-96-354-4649 (A.L.)
                Author information
                https://orcid.org/0000-0002-9397-1003
                Article
                life-09-00021
                10.3390/life9010021
                6463088
                30823538
                c88529e1-25a9-4848-b1a6-2f0af53976cf
                © 2019 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 11 December 2018
                : 19 February 2019
                Categories
                Review

                endosymbiosis,genome-reduction syndrome,consortium,primary endosymbiont,secondary endosymbiont,buchnera,sulcia,tremblaya,symbiotic replacement,minimal genomes

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