McCutcheon JP, Moran NA. Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc Natl Acad Sci USA 104: 19392-19397

Center for Insect Science and Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721-0088, USA.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 01/2008; 104(49):19392-7. DOI: 10.1073/pnas.0708855104
Source: PubMed


Obligate symbioses with nutrient-provisioning bacteria have originated often during animal evolution and have been key to the ecological diversification of many invertebrate groups. To date, genome sequences of insect nutritional symbionts have been restricted to a related cluster within Gammaproteobacteria and have revealed distinctive features, including extreme reduction, rapid evolution, and biased nucleotide composition. Using recently developed sequencing technologies, we show that Sulcia muelleri, a member of the Bacteroidetes, underwent similar genomic changes during coevolution with its sap-feeding insect host (sharpshooters) and the coresident symbiont Baumannia cicadellinicola (Gammaproteobacteria). At 245 kilobases, Sulcia's genome is approximately one tenth of the smallest known Bacteroidetes genome and among the smallest for any cellular organism. Analysis of the coding capacities of Sulcia and Baumannia reveals striking complementarity in metabolic capabilities.

Download full-text


Available from: Nancy A Moran,
  • Source
    • "In the leafhoppers (Cicadellidae), one large group within Auchenorrhyncha, hosts generally harbor two symbionts that have partitioned EAA synthesis. Generally, the oldest associate, Sulcia muelleri (Bacteroidetes), synthesizes eight EAAs, while a diversity of co-­‐resident symbionts are responsible for the remaining two, methionine and histidine (McCutcheon & Moran 2007, 2010; Bennett & Moran 2013; Chang et al., 2015). One of the largest genomes of an insect obligate symbiont sequenced to date belongs to Baumannia cicadellinicola (Gammaproteobacteria) (Fig. 1), which replaced Nasuia deltocephalinicola (Betaproteobacteria) 80-­‐175 million years ago in xylem-­‐feeding sharpshooter leafhoppers (Cicadellinae: Moran et al., 2003; Takiya et al., 2006). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Plant sap-feeding insects (Hemiptera) rely on obligate bacterial symbionts that provision nutrients. Some of these symbionts are ancient and have evolved tiny genomes, while others are younger and retain larger, dynamic genomes. Baumannia cicadellinicola, an obligate symbiont of sharpshooter leafhoppers, is derived from a relatively recent symbiont replacement. To better understand evolutionary decay of genomes, we compared Baumannia from three host species. A newly sequenced genome for Baumannia from the green sharpshooter (B-GSS) was compared to genomes of Baumannia from the blue-green sharpshooter (B-BGSS, 759 kilobases [kb]) and of the glassy-winged sharpshooter (B-GWSS, 680 kb). B-GSS has the smallest Baumannia genome sequenced to date (633 kb), with only three unique genes, all involved in membrane function. It has lost nearly all pathways involved in vitamin and cofactor synthesis, as well as amino acid biosynthetic pathways that are redundant with pathways of the host or the symbiotic partner, Sulcia muelleri. The entire biosynthetic pathway for methionine is eliminated, suggesting that methionine has become a dietary requirement for hosts. B-GSS and B-BGSS share 33 genes involved in bacterial functions (e.g., cell division, membrane synthesis, metabolite transport, etc.) that are lost from the more distantly related B-GWSS and most other tiny genome symbionts. Finally, pairwise divergence estimates indicate that B-GSS has experienced a lineage-specific increase in substitution rates. This increase correlates with accelerated protein-level changes and widespread gene loss. Thus, the mode and tempo of genome reduction vary widely among symbiont lineages and result in wide variation in metabolic capabilities across hosts. © The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
    Genome Biology and Evolution 08/2015; DOI:10.1093/gbe/evv159 · 4.23 Impact Factor
  • Source
    • "Most of these associations have been proven to have a metabolic foundation, where the symbiont provides nutrients that are lacking from the host's diet. This has been established mostly by genomic (Wu et al. 2006; McCutcheon and Moran 2007; Kirkness et al. 2010; Penz et al. 2010; Shigenobu and Wilson 2011; Sloan and Moran 2012; Tokuda et al. 2013), as well as transcriptomic (Hansen and Moran 2011), proteomic (Poliakov et al. 2011; Fan et al. 2013), and in vivo experimental studies (Moran, Dunbar, et al. 2005; Russell et al. 2013). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Particularly interesting cases of mutualistic endosymbioses come from the establishment of co-obligate associations of more than one species of endosymbiotic bacteria. Throughout symbiotic accommodation from a free-living bacterium, passing through a facultative stage and ending as an obligate intracellular one, the symbiont experiences massive genomic losses and phenotypic adjustments. Here, we scrutinized the changes in the co-evolution of Serratia symbiotica and Buchnera aphidicola endosymbionts in aphids, paying particular attention to the transformations undergone by S. symbiotica to become an obligate endosymbiont. While it is already known that S. symbiotica is facultative in Acyrthosiphon pisum, in Cinara cedri it has established a co-obligate endosymbiotic consortium along with B. aphidicola to fulfill the aphid's nutritional requirements. The state of this association in Cinara tujafilina, an aphid belonging to the same subfamily (Lachninae) that C. cedri, remained unknown. Here, we report the genome of S. symbiotica strain SCt-VLC from the aphid C. tujafilina. While being phylogenetically and genomically very closely related to the facultative endosymbiont S. symbiotica from the aphid A. pisum, it shows a variety of metabolic, genetic and architectural features which point towards this endosymbiont being one step closer to an obligate intracellular one. We also describe in depth the process of genome rearrangements suffered by S. symbiotica and the role mobile elements play in gene inactivations. Finally, we postulate the supply to the host of the essential riboflavin (vitamin B2) as key to the establishment of S. symbiotica as a co-obligate endosymbiont in the aphids belonging to the subfamily Lachninane.
    Genome Biology and Evolution 06/2014; 6(7):1683-1698. DOI:10.1093/gbe/evu133 · 4.23 Impact Factor
  • Source
    • "A second factor that could explain the loss of genetic information from bacterial genomes is genetic drift (Andersson and Kurland 1998; Moran 2002; Kuo et al. 2009). When bacteria transition from a free-living to a symbiotic lifestyle such as the bacterial endosymbionts of insects (Ochman and Moran 2001; Moran and Plague 2004; McCutcheon and Moran 2007), repeated bottlenecks of relatively small populations may result in a weakened selection even for required genes, thus resulting in an elimination of dispensable genes (Moran et al. 2008). Indeed, experimentally evolving Salmonella enterica by subjecting it to regular population bottlenecks resulted in a reduction of genome size and a concomitant loss of essential genes (Nilsson et al. 2005). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Bacteria that have adapted to nutrient-rich, stable environments are typically characterized by reduced genomes. The loss of biosynthetic genes frequently renders these lineages auxotroph, hinging their survival on an environmental uptake of certain metabolites. The evolutionary forces that drive this genome degradation, however, remain elusive. Our analysis of 949 metabolic networks revealed auxotrophies are likely highly prevalent in both symbiotic and free-living bacteria. To unravel whether selective advantages can account for the rampant loss of anabolic genes, we systematically determined the fitness consequences that result from deleting conditionally essential biosynthetic genes from the genomes of Escherichia coli and Acinetobacter baylyi in the presence of the focal nutrient. Pairwise competition experiments with each of 20 mutants auxotrophic for different amino acids, vitamins, and nucleobases against the prototrophic wild type unveiled a pronounced, concentration-dependent growth advantage of around 13% for virtually all mutants tested. Individually deleting different genes from the same biosynthesis pathway entailed gene-specific fitness consequences and loss of the same biosynthetic genes from the genomes of E. coli and A. baylyi differentially affected the fitness of the resulting auxotrophic mutants. Taken together, our findings suggest adaptive benefits could drive the loss of conditionally essential biosynthetic genes. This article is protected by copyright. All rights reserved.
    Evolution 06/2014; 68(9). DOI:10.1111/evo.12468 · 4.61 Impact Factor
Show more