A Possible Heterodimeric Prophage-Like Element in the Genome of the Insect Endosymbiont<i>Sodalis glossinidius</i>

Clark, Alvin J.; Pontes, Mauricio H.; Jones, Tait; Dale, Colin

doi:10.1128/jb.00913-06

Cited by 14 publications

(17 citation statements)

References 15 publications

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“…While lysozymes are primarily involved in lysis of the bacterial cell, the lysozyme of phage P22 is also packaged into the virion and is later released after the particle has adsorbed to the host cell, facilitating entry of the phage chromosome (56). This same phenomenon may be present in APSE, since the structural genes involved in the construction of the phage virion and injection of the phage DNA into the bacterial host are orthologous to those in P22 (21,85).…”

Section: Vol 74 2008 Localized Variation In Phage Virulence Cassettmentioning

confidence: 80%

“…Recombination of bacteriophages commonly results in a mosaic genomic architecture in which different gene blocks are highly similar to those of distinct phages (47,49). APSE shares a core block of genes with the nonintegrative bacteriophage SG1 (also termed pSOG3), which infects the facultative endosymbiont of tsetse flies, Sodalis glossinidius (21). In the Sodalis genome, 262 of 2,432 intact ORFs are phage related (83), and numerous degraded prophage elements are homologous to APSE genes (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…However, among facultative (secondary) endosymbionts of insects, several phage have been found (21,44,54,83,85,91). APSE, a lambda-like phage, infects "Candidatus Hamiltonella defensa," a facultative endosymbiont known from a wide range of sap-feeding insects (aphids, mealybugs, psyllids, and whiteflies) (20,22,59,74,77).…”

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Diverse Phage-Encoded Toxins in a Protective Insect Endosymbiont

Degnan

Moran

2008

Appl Environ Microbiol

184

221

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The lysogenic bacteriophage APSE infects "Candidatus Hamiltonella defensa," a facultative endosymbiont of aphids and other sap-feeding insects. This endosymbiont has established a beneficial association with aphids, increasing survivorship following attack by parasitoid wasps. Although APSE and "Ca. Hamiltonella defensa" are effectively maternally transmitted between aphid generations, they can also be horizontally transferred among insect hosts, which results in genetically distinct "Ca. Hamiltonella defensa" strains infecting the same aphid species and sporadic distributions of both APSE and "Ca. Hamiltonella defensa" among hosts. Aphids infected only with "Ca. Hamiltonella defensa" have significantly less protection than those infected with both "Ca. Hamiltonella defensa" and APSE. This protection has been proposed to be connected to eukaryotetargeted toxins previously discovered in the genomes of two characterized APSE strains. In this study, we have sequenced partial genomes from seven additional APSE strains to address the evolution and extent of toxin variation in this phage. The APSE lysis region has been a hot spot for nonhomologous recombination of novel virulence cassettes. We identified four new toxins from three protein families, Shiga-like toxin, cytolethal distending toxin, and YD-repeat toxins. These recombination events have also resulted in reassortment of the downstream lysozyme and holin genes. Analysis of the conserved APSE genes flanking the variable toxin cassettes reveals a close phylogenetic association with phage sequences from two other facultative endosymbionts of insects. Thus, phage may act as a conduit for ongoing gene exchange among heritable endosymbionts.Bacteriophage genomes are in a state of constant flux, reflecting a propensity to undergo rampant recombination (47,49,72). As such, phage are an important vector for horizontal gene transfer (HGT) within and between bacterial species (15,19,63). In addition, integrated temperate phage (prophage) frequently constitute the single greatest source of genomic variation among closely related bacterial strains (9,16,17). This flexible pool of phage-encoded loci has wide-ranging effects that can alter a bacterial host's antigenicity, toxicity, or even metabolic capacity (4,43,87).While infection by multiple phage types is common in freeliving bacteria, phage are completely absent from bacteria with host-restricted lifestyles, such as obligate intracellular mutualists of insects (2,24,60,86,90). However, among facultative (secondary) endosymbionts of insects, several phage have been found (21,44,54,83,85,91). APSE, a lambda-like phage, infects "Candidatus Hamiltonella defensa," a facultative endosymbiont known from a wide range of sap-feeding insects (aphids, mealybugs, psyllids, and whiteflies) (20,22,59,74,77). Pea aphids, Acyrthosiphon pisum (Hemiptera: Aphididae), infected with "Ca. Hamiltonella defensa" and APSE are significantly more successful at surviving attempted parasitism by the solitary endoparasitoid wasps Aphidius ervi an...

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Section: Vol 74 2008 Localized Variation In Phage Virulence Cassettmentioning

confidence: 80%

Section: Discussionmentioning

confidence: 99%

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Diverse Phage-Encoded Toxins in a Protective Insect Endosymbiont

Degnan

Moran

2008

Appl Environ Microbiol

184

221

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“…Here, we report the first instance of phage encoding the factors directly underlying a mutualistic symbiosis. Whereas obligate symbionts, such as Buchnera aphidicola , have greatly reduced and static genomes, with no evidence of ongoing horizontal gene transfer, facultative inherited symbionts, including Wolbachia , have been found to carry several mobile elements (14, 20–22). Our results show that mobile genetic elements can endow a bacterial symbiont with beneficial functions that extend to the eukaryotic host.…”

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confidence: 99%

Bacteriophages Encode Factors Required for Protection in a Symbiotic Mutualism

Oliver¹,

Degnan

Hunter

et al. 2009

Science

418

414

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Bacteriophages are known to carry key virulence factors for pathogenic bacteria, but their roles in symbiotic bacteria are less well understood. The heritable symbiont Hamiltonella defensa protects the aphid Acyrthosiphon pisum from attack by the parasitoid Aphidius ervi by killing developing wasp larvae. In a controlled genetic background, we show that a toxin-encoding bacteriophage is required to produce the protective phenotype. Phage loss occurs repeatedly in laboratory-held H. defensa–infected aphid clonal lines, resulting in increased susceptibility to parasitism in each instance. Our results show that these mobile genetic elements can endow a bacterial symbiont with benefits that extend to the animal host. Thus, phages vector ecologically important traits, such as defense against parasitoids, within and among symbiont and animal host lineages.

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“…Thirty-three of these sequences have intact or largely intact virion morphogenetic gene clusters. The details of the bio-informatic analysis of these phage genomes will be described elsewhere, but we note here that phages P22,18 Sf6,19 CUS-3,20 φSG121; 22 and APSE-123 are prototypic of five subgroups within the P22-like phages that have, for example, very large differences among their procapsid assembly and terminase protein (S. Casjens, in preparation). The 14% identity between the coat proteins of phages P22 and Sf6, for example, demonstrates that the genes of these five types have been diverging for a very long time.…”

Section: Resultsmentioning

confidence: 99%

An Evolutionarily Conserved Family of Virion Tail Needles Related to Bacteriophage P22 gp26: Correlation between Structural Stability and Length of the α-Helical Trimeric Coiled Coil

Bhardwaj

Walker-Kopp

Casjens

et al. 2009

Journal of Molecular Biology

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Bacteriophages of the Podoviridae family use short non-contractile tails to inject their genetic material into Gram-negative bacteria. In phage P22, the tail contains a thin needle, encoded by the phage gene 26, which is essential both for stabilization and ejection of the packaged viral genome. Bio-informatic analysis of the N-terminal domain of gp26 (residues 1–60) led us to identify a family of genes encoding putative homologues of the tail needle gp26. To validate this idea experimentally and to explore their diversity, we cloned the gp26-like gene from phages HK620, Sf6, HS1, and characterized these gene products in solution. All gp26-like factors contain an elongated α-helical coiled-coil core consisting of repeating, adjacent trimerization heptads and form trimeric fibers with length ranging between about 240Å to 300Å. Gp26-tail needles display high structural stability in solution, with Tm (temperature of melting) between 85–95°C. To determine how the structural stability of these phage fibers correlates with the length of the α-helical core, we investigated the effect of insertions and deletions in the helical core. In P22 tail needle, we identified an 85-residue long helical domain, termed MiCRU (Minimal Coiled-coil Repeat Unit), that can be inserted in frame inside gp26 helical core, preserving the straight morphology of the fiber. Likewise, we were able to remove three quarters of the helical core of HS1 tail needle minimally decreasing the stability of the fiber. We conclude that in the gp26 family of tail needles, structural stability increases non-linearly with the length of the α-helical core. Thus, the overall stability of these bacteriophage fibers is not solely dependent on the number of trimerization repeats in the α-helical core.

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A Possible Heterodimeric Prophage-Like Element in the Genome of the Insect EndosymbiontSodalis glossinidius

Cited by 14 publications

References 15 publications

Diverse Phage-Encoded Toxins in a Protective Insect Endosymbiont

Diverse Phage-Encoded Toxins in a Protective Insect Endosymbiont

Bacteriophages Encode Factors Required for Protection in a Symbiotic Mutualism

An Evolutionarily Conserved Family of Virion Tail Needles Related to Bacteriophage P22 gp26: Correlation between Structural Stability and Length of the α-Helical Trimeric Coiled Coil

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