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      Differential Genome Evolution Between Companion Symbionts in an Insect-Bacterial Symbiosis

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          ABSTRACT

          Obligate symbioses with bacteria allow insects to feed on otherwise unsuitable diets. Some symbionts have extremely reduced genomes and have lost many genes considered to be essential in other bacteria. To understand how symbiont genome degeneration proceeds, we compared the genomes of symbionts in two leafhopper species, Homalodisca vitripennis (glassy-winged sharpshooter [GWSS]) and Graphocephala atropunctata (blue-green sharpshooter [BGSS]) (Hemiptera: Cicadellidae). Each host species is associated with the anciently acquired “ Candidatus Sulcia muelleri” ( Bacteroidetes) and the more recently acquired “ Candidatus Baumannia cicadellinicola” ( Gammaproteobacteria). BGSS “ Ca. Baumannia” retains 89 genes that are absent from GWSS “ Ca. Baumannia”; these underlie central cellular functions, including cell envelope biogenesis, cellular replication, and stress response. In contrast, “ Ca. Sulcia” strains differ by only a few genes. Although GWSS “ Ca. Baumannia” cells are spherical or pleomorphic (a convergent trait of obligate symbionts), electron microscopy reveals that BGSS “ Ca. Baumannia” maintains a rod shape, possibly due to its retention of genes involved in cell envelope biogenesis and integrity. Phylogenomic results suggest that “ Ca. Baumannia” is derived from the clade consisting of Sodalis and relatives, a group that has evolved symbiotic associations with numerous insect hosts. Finally, the rates of synonymous and nonsynonymous substitutions are higher in “ Ca. Baumannia” than in “ Ca. Sulcia,” which may be due to a lower mutation rate in the latter. Taken together, our results suggest that the two “ Ca. Baumannia” genomes represent different stages of genome reduction in which many essential functions are being lost and likely compensated by hosts. “ Ca. Sulcia” exhibits much greater genome stability and slower sequence evolution, although the mechanisms underlying these differences are poorly understood.

          IMPORTANCE

          In obligate animal-bacterial symbioses, bacteria experience extreme patterns of genome evolution, including massive gene loss and rapid evolution. However, little is known about this process, particularly in systems with complementary bacterial partners. To understand whether genome evolution impacts symbiont types equally and whether lineages follow the same evolutionary path, we sequenced the genomes of two coresident symbiotic bacteria from a plant sap-feeding insect and compared them to the symbionts from a related host species. We found that the older symbiont has a highly reduced genome with low rates of mutation and gene loss. In contrast, the younger symbiont has a larger genome that exhibits higher mutation rates and varies dramatically in the retention of genes related to cell wall biogenesis, cellular replication, and stress response. We conclude that while symbiotic bacteria evolve toward tiny genomes, this process is shaped by different selection intensities that may reflect the different ages and metabolic roles of symbiont types.

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          Most cited references72

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          Is Open Access

          TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations

          We present TranslatorX, a web server designed to align protein-coding nucleotide sequences based on their corresponding amino acid translations. Many comparisons between biological sequences (nucleic acids and proteins) involve the construction of multiple alignments. Alignments represent a statement regarding the homology between individual nucleotides or amino acids within homologous genes. As protein-coding DNA sequences evolve as triplets of nucleotides (codons) and it is known that sequence similarity degrades more rapidly at the DNA than at the amino acid level, alignments are generally more accurate when based on amino acids than on their corresponding nucleotides. TranslatorX novelties include: (i) use of all documented genetic codes and the possibility of assigning different genetic codes for each sequence; (ii) a battery of different multiple alignment programs; (iii) translation of ambiguous codons when possible; (iv) an innovative criterion to clean nucleotide alignments with GBlocks based on protein information; and (v) a rich output, including Jalview-powered graphical visualization of the alignments, codon-based alignments coloured according to the corresponding amino acids, measures of compositional bias and first, second and third codon position specific alignments. The TranslatorX server is freely available at http://translatorx.co.uk.
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            Extreme genome reduction in symbiotic bacteria.

            Since 2006, numerous cases of bacterial symbionts with extraordinarily small genomes have been reported. These organisms represent independent lineages from diverse bacterial groups. They have diminutive gene sets that rival some mitochondria and chloroplasts in terms of gene numbers and lack genes that are considered to be essential in other bacteria. These symbionts have numerous features in common, such as extraordinarily fast protein evolution and a high abundance of chaperones. Together, these features point to highly degenerate genomes that retain only the most essential functions, often including a considerable fraction of genes that serve the hosts. These discoveries have implications for the concept of minimal genomes, the origins of cellular organelles, and studies of symbiosis and host-associated microbiota.
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              Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models.

              Q. Z. Yang (2000)
              Approximate methods for estimating the numbers of synonymous and nonsynonymous substitutions between two DNA sequences involve three steps: counting of synonymous and nonsynonymous sites in the two sequences, counting of synonymous and nonsynonymous differences between the two sequences, and correcting for multiple substitutions at the same site. We examine complexities involved in those steps and propose a new approximate method that takes into account two major features of DNA sequence evolution: transition/transversion rate bias and base/codon frequency bias. We compare the new method with maximum likelihood, as well as several other approximate methods, by examining infinitely long sequences, performing computer simulations, and analyzing a real data set. The results suggest that when there are transition/transversion rate biases and base/codon frequency biases, previously described approximate methods for estimating the nonsynonymous/synonymous rate ratio may involve serious biases, and the bias can be both positive and negative. The new method is, in general, superior to earlier approximate methods and may be useful for analyzing large data sets, although maximum likelihood appears to always be the method of choice.
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                Author and article information

                Journal
                mBio
                MBio
                mbio
                mbio
                mBio
                mBio
                American Society of Microbiology (1752 N St., N.W., Washington, DC )
                2150-7511
                30 September 2014
                Sep-Oct 2014
                : 5
                : 5
                : e01697-14
                Affiliations
                [ a ]Department of Integrative Biology, University of Texas, Austin, Texas, USA
                [ b ]Division of Biological Sciences, University of Montana, Missoula, Montana, USA
                [ c ]Department of Bacteriology, University of Wisconsin—Madison, Madison, Wisconsin, USA
                [ d ]Institute for Cellular and Molecular Biology, University of Texas, Austin, Texas, USA
                Author notes
                Address correspondence to Gordon M. Bennett, gordon.bennett@ 123456utexas.edu .

                Editor Margaret J. McFall-Ngai, University of Wisconsin

                Article
                mBio01697-14
                10.1128/mBio.01697-14
                4196230
                25271287
                e6ed0285-d152-47df-bf94-6d7c8d895e11
                Copyright © 2014 Bennett et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 23 July 2014
                : 26 August 2014
                Page count
                Pages: 12
                Categories
                Research Article
                Custom metadata
                September/October 2014

                Life sciences
                Life sciences

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