Degnan PH, Yu Y, Sisneros N, Wing RA, Moran NA.. Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proc Natl Acad Sci USA 106: 9063-9068

Department of Ecology and Evolutionary Biology, Arizona Genomics Institute, University of Arizona, Tucson, AZ 85721. USA.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 06/2009; 106(22):9063-8. DOI: 10.1073/pnas.0900194106
Source: PubMed


Eukaryotes engage in a multitude of beneficial and deleterious interactions with bacteria. Hamiltonella defensa, an endosymbiont of aphids and other sap-feeding insects, protects its aphid host from attack by parasitoid wasps. Thus H. defensa is only conditionally beneficial to hosts, unlike ancient nutritional symbionts, such as Buchnera, that are obligate. Similar to pathogenic bacteria, H. defensa is able to invade naive hosts and circumvent host immune responses. We have sequenced the genome of H. defensa to identify possible mechanisms that underlie its persistence in healthy aphids and protection from parasitoids. The 2.1-Mb genome has undergone significant reduction in size relative to its closest free-living relatives, which include Yersinia and Serratia species (4.6-5.4 Mb). Auxotrophic for 8 of the 10 essential amino acids, H. defensa is reliant upon the essential amino acids produced by Buchnera. Despite these losses, the H. defensa genome retains more genes and pathways for a variety of cell structures and processes than do obligate symbionts, such as Buchnera. Furthermore, putative pathogenicity loci, encoding type-3 secretion systems, and toxin homologs, which are absent in obligate symbionts, are abundant in the H. defensa genome, as are regulatory genes that likely control the timing of their expression. The genome is also littered with mobile DNA, including phage-derived genes, plasmids, and insertion-sequence elements, highlighting its dynamic nature and the continued role horizontal gene transfer plays in shaping it.

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    • "The predator gut appears to be suitable for initial high rates of reproduction of these symbionts, suggestive of an infection attempt during the 3 h after A. pisum ingestion. Indeed, Degnan et al. (2009) found that H. defensa had abundant putative pathogenicity loci and regulatory genes that may be important for infecting new hosts. In addition, Costopoulos et al. (2014) fed the coccinellid Hippodamia convergens with aphids containing either H. defensa or S. symbiotica which, compared to a control diet, reduced coccinellid survival and increased adult size. "
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    ABSTRACT: DNA methods are useful to identify ingested prey items from the gut of predators, but reliable detection is hampered by low amounts of degraded DNA. PCR-based methods can retrieve minute amounts of starting material but suffer from amplification biases and cross-reactions with the predator and related species genomes. Here, we use PCR-free direct shotgun sequencing of total DNA isolated from the gut of the harlequin ladybird Harmonia axyridis at five time points after feeding on a single pea aphid Acyrthosiphon pisum. Sequence reads were matched to three reference databases: Insecta mitogenomes of 587 species, including H. axyridis sequenced here; A. pisum nuclear genome scaffolds; and scaffolds and complete genomes of 13 potential bacterial symbionts. Immediately after feeding, multicopy mtDNA of A. pisum was detected in tens of reads, while hundreds of matches to nuclear scaffolds were detected. Aphid nuclear DNA and mtDNA decayed at similar rates (0.281 and 0.11 h−1 respectively), and the detectability periods were 32.7 and 23.1 h. Metagenomic sequencing also revealed thousands of reads of the obligate Buchnera aphidicola and facultative Regiella insecticola aphid symbionts, which showed exponential decay rates significantly faster than aphid DNA (0.694 and 0.80 h−1 respectively). However, the facultative aphid symbionts Hamiltonella defensa, Arsenophonus spp. and Serratia symbiotica showed an unexpected temporary increase in population size by 1-2 orders of magnitude in the predator guts before declining. Metagenomics is a powerful tool that can reveal complex relationships and the dynamics of interactions among predators, prey and their symbionts.This article is protected by copyright. All rights reserved.
    Molecular Ecology Resources 12/2014; 15(4). DOI:10.1111/1755-0998.12364 · 3.71 Impact Factor
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    • "Along with B. aphidicola, many aphids can also harbor a variety of other " more recently " acquired secondary endosymbionts , such as Regiella insecticola (Degnan et al. 2009), Hamiltonella defensa (Degnan, Yu, et al. 2009), Rickettsia (Sakurai et al. 2005), Rickettsiella viridis (Tsuchida et al. 2014), Wolbachia (Gó mez-Valero et al. 2004), and Serratia symbiotica (Moran, Russell, et al. 2005). These secondary endosymbionts generally display characteristics contrasting those of ancient obligate (also called primary) endosymbionts, including a lower coding density, presence of mobile genetic elements, larger genome sizes, a higher G+C content, and a high number of pseudogenes (Degnan et al. 2009; Newton and Bordenstein 2011; Oakeson et al. 2014). "
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    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
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    • "S3, Supplementary Material online). The complete sets of genes required for the synthesis of both cofactors was described for the Hamiltonella secondary endosymbiont of the aphid Acyrthosiphon pisum (Degnan et al. 2009), and all of them were also found by BLAST similarity in the draft genome of Hamiltonella from B. tabaci strain QHC-VLC (unpublished data). "
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    ABSTRACT: Many insects harbour inherited bacterial endosymbionts. Although some of them are not strictly essential and are considered facultative, they can be a key to host survival under specific environmental conditions, such as parasitoid attacks, climate changes or insecticide pressures. The whitefly Bemisia tabaci is top of the list of organisms inflicting agricultural damage and outbreaks, and changes in its distribution may be associated to global warming. In this work, we have sequenced and analysed the genome of Cardinium cBtQ1, a facultative bacterial endosymbiont of B. tabaci and propose that it belongs to a new taxonomic family, which also includes Candidatus Amoebophilus asiaticus and Cardinium cEper1, endosymbionts of amoeba and wasps, respectively. Reconstruction of their last common ancestors' gene contents revealed an initial massive gene loss from the free-living ancestor. This was followed in Cardinium by smaller losses, associated with settlement in arthropods. Some of these losses, affecting cofactor and amino acid biosynthetic encoding genes, took place in Cardinium cBtQ1 after its divergence from the Cardinium cEper1 lineage and were related to its settlement in the whitefly and its endosymbionts. Furthermore, the Cardinium cBtQ1 genome displays a large proportion of transposable elements, which have recently inactivated genes and produced chromosomal rearrangements. The genome also contains a chromosomal duplication and a multicopy plasmid, which harbours several genes putatively associated with gliding motility, as well as two other genes encoding proteins with potential insecticidal activity. As gene amplification is very rare in endosymbionts, an important function of these genes cannot be ruled out.
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