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      Genome Reduction in the Mosquito Symbiont Asaia

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          Abstract

          Symbiosis is now recognized as a driving force in evolution, a role that finds its ultimate expression in the variety of associations bonding insects with microbial symbionts. These associations have contributed to the evolutionary success of insects, with the hosts acquiring the capacity to exploit novel ecological niches, and the symbionts passing from facultative associations to obligate, mutualistic symbioses. In bacterial symbiont of insects, the transition from the free-living life style to mutualistic symbiosis often resulted in a reduction in the genome size, with the generation of the smallest bacterial genomes thus far described. Here, we show that the process of genome reduction is still occurring in Asaia, a group of bacterial symbionts associated with a variety of insects. Indeed, comparative genomics of Asaia isolated from different mosquito species revealed a substantial genome size and gene content reduction in Asaia from Anopheles darlingi, a South-American malaria vector. We thus propose Asaia as a novel model to study genome reduction dynamics, within a single bacterial taxon, evolving in a common biological niche.

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          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.
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            Why do species vary in their rate of molecular evolution?

            Despite hopes that the processes of molecular evolution would be simple, clock-like and essentially universal, variation in the rate of molecular evolution is manifest at all levels of biological organization. Furthermore, it has become clear that rate variation has a systematic component: rate of molecular evolution can vary consistently with species body size, population dynamics, lifestyle and location. This suggests that the rate of molecular evolution should be considered part of life-history variation between species, which must be taken into account when interpreting DNA sequence differences between lineages. Uncovering the causes and correlates of rate variation may allow the development of new biologically motivated models of molecular evolution that may improve bioinformatic and phylogenetic analyses.
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              Genome reduction and co-evolution between the primary and secondary bacterial symbionts of psyllids.

              Genome reduction in obligately intracellular bacteria is one of the most well-established patterns in the field of molecular evolution. In the extreme, many sap-feeding insects harbor nutritional symbionts with genomes that are so reduced that it is not clear how they perform basic cellular functions. For example, the primary symbiont of psyllids (Carsonella) maintains one of the smallest and most AT-rich bacterial genomes ever identified and has surprisingly lost many genes that are thought to be essential for its role in provisioning its host with amino acids. However, our understanding of this extreme case of genome reduction is limited, as genomic data for Carsonella are available from only a single host species, and little is known about the functional role of "secondary" bacterial symbionts in psyllids. To address these limitations, we analyzed complete Carsonella genomes from pairs of congeneric hosts in three divergent genera within the Psyllidae (Ctenarytaina, Heteropsylla, and Pachypsylla) as well as complete secondary symbiont genomes from two of these host species (Ctenarytaina eucalypti and Heteropsylla cubana). Although the Carsonella genomes are generally conserved in size, structure, and GC content and exhibit genome-wide signatures of purifying selection, we found that gene loss has remained active since the divergence of the host species and had a particularly large impact on the amino acid biosynthesis pathways that define the symbiotic role of Carsonella. In some cases, the presence of additional bacterial symbionts may compensate for gene loss in Carsonella, as functional gene content indicates a high degree of metabolic complementarity between co-occurring symbionts. The genomes of the secondary symbionts also show signatures of long-term evolution as vertically transmitted, intracellular bacteria, including more extensive genome reduction than typically observed in facultative symbionts. Therefore, a history of co-evolution with secondary bacterial symbionts can partially explain the ongoing genome reduction in Carsonella. However, the absence of these secondary symbionts in other host lineages indicates that the relationships are dynamic and that other mechanisms, such as changes in host diet or functional coordination with the host genome, must also be at play.
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                Author and article information

                Contributors
                Role: Associate Editor
                Journal
                Genome Biol Evol
                Genome Biol Evol
                gbe
                Genome Biology and Evolution
                Oxford University Press
                1759-6653
                January 2019
                23 November 2018
                23 November 2018
                : 11
                : 1
                : 1-10
                Affiliations
                [1 ]Biotechnology Institute (IBTEC) & Biosciences Institute at Botucatu (IBB), Sao Paulo State University (UNESP), Sao Paulo, Brazil
                [2 ]School of Biosciences and Veterinary Medicine, University of Camerino, Italy
                [3 ]Clinical Pediatric Research Center Romeo and Enrica Invernizzi, Department of Biosciences, University of Milan, Italy
                [4 ]MRC-University of Glasgow-Centre for Virus Research, Glasgow, United Kingdom
                Author notes

                These authors contributed equally to this work.

                Data deposition: The project has been deposited at NCBI BioProject database under the accession number PRJNA454517.

                Author information
                http://orcid.org/0000-0002-4420-8482
                Article
                evy255
                10.1093/gbe/evy255
                6317953
                30476071
                11307e94-ee74-4057-8df0-afdea635f50d
                © The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 21 November 2018
                Page count
                Pages: 10
                Funding
                Funded by: PRIN
                Award ID: 2012T85B3R_001
                Award ID: 2015JXC3JF_001
                Funded by: Italian Ministry of Education, University and Research
                Funded by: University of Camerino
                Categories
                Research Article

                Genetics
                anopheles darlingi,asaia,symbiosis,genome reduction
                Genetics
                anopheles darlingi, asaia, symbiosis, genome reduction

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