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      Genomic revelations of a mutualism: the pea aphid and its obligate bacterial symbiont

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          Abstract

          The symbiosis of the pea aphid Acyrthosphion pisum with the bacterium Buchnera aphidicola APS represents the best-studied insect obligate symbiosis. Here we present a refined picture of this symbiosis by linking pre-genomic observations to new genomic data that includes the complete genomes of the eukaryotic and prokaryotic symbiotic partners. In doing so, we address four issues central to understanding the patterns and processes operating at the A. pisum/ Buchnera APS interface. These four issues include: (1) lateral gene transfer, (2) host immunity, (3) symbiotic metabolism, and (4) regulation.

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          The online version of this article (doi:10.1007/s00018-011-0645-2) contains supplementary material, which is available to authorized users.

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          Most cited references74

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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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            Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae).

            Polymerase chain reaction (PCR) products corresponding to 803 bp of the cytochrome oxidase subunits I and II region of mitochondrial DNA (mtDNA COI-II) were deduced to consist of multiple haplotypes in three Sitobion species. We investigated the molecular basis of these observations. PCR products were cloned, and six clones from one individual per species were sequenced. In each individual, one sequence was found commonly, but also two or three divergent sequences were seen. The divergent sequences were shown to be nonmitochondrial by sequencing from purified mtDNA and Southern blotting experiments. All seven nonmitochondrial clones sequenced to completion were unique. Nonmitochondrial sequences have a high proportion of unique sites, and very few characters are shared between nonmitochondrial clones to the exclusion of mtDNA. From these data, we infer that fragments of mtDNA have been transposed separately (probably into aphid chromosomes), at a frequency only known to be equalled in humans. The transposition phenomenon appears to occur infrequently or not at all in closely related genera and other aphids investigated. Patterns of nucleotide substitution in mtDNA inferred over a parsimony tree are very different from those in transposed sequences. Compared with mtDNA, nonmitochondrial sequences have less codon position bias, more even exchanges between A, G, C and T, and a higher proportion of nonsynonymous replacements. Although these data are consistent with the transposed sequences being under less constraint than mtDNA, changes in the nonmitochondrial sequences are not random: there remains significant position bias, and probable excesses of synonymous replacements and of conservative inferred amino acid replacements. We conclude that a proportion of the inferred change in the nonmitochondrial sequences occurred before transposition. We believe that Sitobion aphids (and other species exhibiting mtDNA transposition) may be important for studying the molecular evolution of mtDNA and pseudogenes. However, our data highlight the need to establish the true evolutionary relationships between sequences in comparative investigations.
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              The genome sequence of Rickettsia prowazekii and the origin of mitochondria.

              We describe here the complete genome sequence (1,111,523 base pairs) of the obligate intracellular parasite Rickettsia prowazekii, the causative agent of epidemic typhus. This genome contains 834 protein-coding genes. The functional profiles of these genes show similarities to those of mitochondrial genes: no genes required for anaerobic glycolysis are found in either R. prowazekii or mitochondrial genomes, but a complete set of genes encoding components of the tricarboxylic acid cycle and the respiratory-chain complex is found in R. prowazekii. In effect, ATP production in Rickettsia is the same as that in mitochondria. Many genes involved in the biosynthesis and regulation of biosynthesis of amino acids and nucleosides in free-living bacteria are absent from R. prowazekii and mitochondria. Such genes seem to have been replaced by homologues in the nuclear (host) genome. The R. prowazekii genome contains the highest proportion of non-coding DNA (24%) detected so far in a microbial genome. Such non-coding sequences may be degraded remnants of 'neutralized' genes that await elimination from the genome. Phylogenetic analyses indicate that R. prowazekii is more closely related to mitochondria than is any other microbe studied so far.
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                Author and article information

                Contributors
                +81-564-557670 , +81-564-557669 , shige@nibb.ac.jp
                Journal
                Cell Mol Life Sci
                Cellular and Molecular Life Sciences
                SP Birkhäuser Verlag Basel (Basel )
                1420-682X
                1420-9071
                10 March 2011
                10 March 2011
                April 2011
                : 68
                : 8
                : 1297-1309
                Affiliations
                [1 ]NIBB Core Research Facilities, National Institute for Basic Biology, Myodaiji, Okazaki 444-8585 Japan
                [2 ]PRESTO, JST, 4-1-8 Honcho Kawaguchi, Saitama, 332-0012 Japan
                [3 ]Department of Biology, University of Miami, Coral Gables, FL 33146 USA
                Article
                645
                10.1007/s00018-011-0645-2
                3064905
                21390549
                fbe87a7e-52ee-4cca-ad16-4250b8b3f7e6
                © The Author(s) 2011
                History
                : 10 February 2011
                : 15 February 2011
                : 15 February 2011
                Categories
                Multi-Author Review
                Custom metadata
                © Springer Basel AG 2011

                Molecular biology
                lateral gene transfer,bacteriocyte,symbiosis,amino acid metabolism,regulation,buchnera

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