Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle

Kirkness, Ewen F.; Haas, Brian J.; Sun, Weilin; Braig, Henk R.; Perotti, M. Alejandra; Clark, J. Marshall; Lee, Si Hyeock; Robertson, Hugh M.; Kennedy, Ryan; Elhaik, Eran; Gerlach, Daniel; Kriventseva, Evgenia V.; Elsik, Christine G.; Graur, Dan; Hill, Catherine A.; Veenstra, Jan A.; Walenz, Brian P.; Tubío, José M. C.; Ribeiro, José M. C.; Rozas, Julio; Johnston, J. Spencer; Reese, Justin; Popadić, Aleksandar; Tojo, Marta; Raoult, Didier; Reed, David L.; Tomoyasu, Yoshinori; Kraus, E. B.; Mittapalli, Omprakash; Margam, Venu M.; Li, Hongmei; Meyer, Jason M.; Johnson, Reed M.; Romero‐Severson, Jeanne; VanZee, Janice Pagel; Alvarez‐Ponce, David; Vieira, Filipe Garrett; Aguadé, Montserrat; Guirao-Rico, Sara; Anzola, Juan Manuel; Yoon, Kyong Sup; Strycharz, Joseph P.; Unger, Maria; Christley, Scott; Lobo, Neil F.; Seufferheld, Manfredo J.; Wang, NaiKuan; Dasch, Gregory A.; Struchiner, Cláudio J.; Madey, Gregory R.; Hannick, Linda I.; Bidwell, Shelby L.; Joardar, Vinita; Caler, Elisabet; Shao, Renfu; Barker, Stephen C.; Cameron, Stephen L.; Bruggner, Robert V.; Regier, Allison; Johnson, Justin; Viswanathan, Lakshmi; Utterback, Terry; Sutton, Granger; Lawson, Daniel; Waterhouse, Robert M.; Venter, J. Craig; Strausberg, Robert L.; Berenbaum, May R.; Collins, Frank H.; Zdobnov, Evgeny M.; Pittendrigh, Barry R.

doi:10.1073/pnas.1003379107

Cited by 481 publications

(478 citation statements)

References 67 publications

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“…Symbiont-mediated provisioning of riboflavin has been experimentally demonstrated or suggested in aphid-Buchnera, tsetse-Wigglesworthia, louse-Riesia, and other insect-bacterium symbiotic associations (17)(18)(19), and the complete synthetic pathway for riboflavin is consistently retained in these endosymbiont genomes (3,4,20) and also in most of the Wolbachia genomes determined to date (Fig. 2B).…”

Section: Wcle-provisioned Biotin Significantly Contributes To Fitnessmentioning

confidence: 95%

Evolutionary origin of insect– Wolbachia nutritional mutualism

Nikoh

Hosokawa

Moriyama

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

345

383

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Obligate insect-bacterium nutritional mutualism is among the most sophisticated forms of symbiosis, wherein the host and the symbiont are integrated into a coherent biological entity and unable to survive without the partnership. Originally, however, such obligate symbiotic bacteria must have been derived from free-living bacteria. How highly specialized obligate mutualisms have arisen from less specialized associations is of interest. Here we address this evolutionary issue by focusing on an exceptional insect-Wolbachia nutritional mutualism. Although Wolbachia endosymbionts are ubiquitously found in diverse insects and generally regarded as facultative/parasitic associates for their insect hosts, a Wolbachia strain associated with the bedbug Cimex lectularius, designated as wCle, was shown to be essential for host's growth and reproduction via provisioning of B vitamins. We determined the 1,250,060-bp genome of wCle, which was generally similar to the genomes of insect-associated facultative Wolbachia strains, except for the presence of an operon encoding the complete biotin synthetic pathway that was acquired via lateral gene transfer presumably from a coinfecting endosymbiont Cardinium or Rickettsia. Nutritional and physiological experiments, in which wCle-infected and wCle-cured bedbugs of the same genetic background were fed on B-vitaminmanipulated blood meals via an artificial feeding system, demonstrated that wCle certainly synthesizes biotin, and the wCleprovisioned biotin significantly contributes to the host fitness. These findings strongly suggest that acquisition of a single gene cluster consisting of biotin synthesis genes underlies the bedbug-Wolbachia nutritional mutualism, uncovering an evolutionary transition from facultative symbiosis to obligate mutualism facilitated by lateral gene transfer in an endosymbiont lineage.

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Section: Wcle-provisioned Biotin Significantly Contributes To Fitnessmentioning

confidence: 95%

Evolutionary origin of insect– Wolbachia nutritional mutualism

Nikoh

Hosokawa

Moriyama

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

345

383

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“…It is conceivable that the nycteribiid endosymbiont has a similar role for the host insect. Endosymbiont genome analyses revealed that biosynthetic genes for B vitamins are encoded in the main chromosome of Wigglesworthia (Akman et al, 2002) while present in a plasmid of Riesia (Kirkness et al, 2010). Sequencing of the genome of the nycteribiid endosymbiont will provide a crucial insight into its biological function, in particular involvement in provisioning of B vitamins.…”

Section: Discussionmentioning

confidence: 99%

Reductive genome evolution, host–symbiont co-speciation and uterine transmission of endosymbiotic bacteria in bat flies

et al. 2011

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Bat flies of the family Nycteribiidae are known for their extreme morphological and physiological traits specialized for ectoparasitic blood-feeding lifestyle on bats, including lack of wings, reduced head and eyes, adenotrophic viviparity with a highly developed uterus and milk glands, as well as association with endosymbiotic bacteria. We investigated Japanese nycteribiid bat flies representing 4 genera, 8 species and 27 populations for their bacterial endosymbionts. From all the nycteribiid species examined, a distinct clade of gammaproteobacteria was consistently detected, which was allied to endosymbionts of other insects such as Riesia spp. of primate lice and Arsenophonus spp. of diverse insects. In adult insects, the endosymbiont was localized in specific bacteriocytes in the abdomen, suggesting an intimate host-symbiont association. In adult females, the endosymbiont was also found in the cavity of milk gland tubules, which suggests uterine vertical transmission of the endosymbiont to larvae through milk gland secretion. In adult females of Penicillidia jenynsii, we discovered a previously unknown type of symbiotic organ in the Nycteribiidae: a pair of large bacteriomes located inside the swellings on the fifth abdominal ventral plate. The endosymbiont genes consistently exhibited adenine/thymine biased nucleotide compositions and accelerated rates of molecular evolution. The endosymbiont genome was estimated to be highly reduced, B0.76 Mb in size. The endosymbiont phylogeny perfectly mirrored the host insect phylogeny, indicating strict vertical transmission and host-symbiont co-speciation in the evolutionary course of the Nycteribiidae. The designation 'Candidatus Aschnera chinzeii' is proposed for the endosymbiont clade.

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“…The predicted proteomes in the DBM genome and those from the genomes of 11 insect species 13,14,[64][65][66][67][68][69][70][71] and 1 Arachnida outgroup species 72 were used in BLAST (1 × 10 −7 ). The fragmental alignments of HSPs were joined using Solar 36 .…”

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confidence: 99%

A heterozygous moth genome provides insights into herbivory and detoxification

et al. 2013

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l e t t e r sHow an insect evolves to become a successful herbivore is of profound biological and practical importance. Herbivores are often adapted to feed on a specific group of evolutionarily and biochemically related host plants 1 , but the genetic and molecular bases for adaptation to plant defense compounds remain poorly understood 2 . We report the first whole-genome sequence of a basal lepidopteran species, Plutella xylostella, which contains 18,071 protein-coding and 1,412 unique genes with an expansion of gene families associated with perception and the detoxification of plant defense compounds. A recent expansion of retrotransposons near detoxification-related genes and a wider system used in the metabolism of plant defense compounds are shown to also be involved in the development of insecticide resistance. This work shows the genetic and molecular bases for the evolutionary success of this worldwide herbivore and offers wider insights into insect adaptation to plant feeding, as well as opening avenues for more sustainable pest management.The global pest P. xylostella (Lepidoptera: Yponomeutidae) is thought to have coevolved with the crucifer plant family 3 ( Supplementary Fig. 1) and has become the most destructive pest of economically important food crops, including rapeseed, cauliflower and cabbage 4 . Recently, the total cost of damage and management worldwide was estimated at $4-5 billion per annum 5,6 . This insect is the first species to have evolved resistance to dichlorodiphenyltrichloroethane (DDT) in the 1950s 7 and to Bacillus thuringiensis (Bt) toxins in the 1990s 8 and has developed resistance to all classes of insecticide, making it increasingly difficult to control 9,10 . P. xylostella provides an exceptional system for understanding the genetic and molecular bases of how insect herbivores cope with the broad range of plant defenses and chemicals encountered in the environment (Supplementary Fig. 2).We used a P. xylostella strain (Fuzhou-S) collected from a field in Fuzhou in southeastern China (26.08 °N, 119.28 °E) for sequencing ( Supplementary Fig. 1). Whole-genome shotgun-based Illumina sequencing of single individuals (Supplementary Table 1), even after ten generations of laboratory inbreeding, resulted in a poor initial assembly (N50 = 2.4 kb, representing the size above which 50% of the total length of the sequences is included), owing to high levels of heterozygosity ( Supplementary Figs. 3 and 4 and Supplementary Table 2). Subsequently, we sequenced 100,800 fosmid clones (comprising ~10× the genome length) to a depth of 200× ( Supplementary Fig. 5 and Supplementary Tables 3-5), assembling the resulting sequence data into 1,819 scaffolds, with an N50 of 737 kb, spanning ~394 Mb of the genome sequence (version 1; Supplementary Fig. 6 and Supplementary Table 6). The assembly covered 85.5% of a set of protein-coding ESTs (Supplementary Tables 7 and 8) generated by transcriptome sequencing 11 . Alignment of a subject scaffold against a 126-kb BAC (GenBank GU058050) from an altern...

show abstract

Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle

Cited by 481 publications

References 67 publications

Evolutionary origin of insect– Wolbachia nutritional mutualism

Evolutionary origin of insect– Wolbachia nutritional mutualism

Reductive genome evolution, host–symbiont co-speciation and uterine transmission of endosymbiotic bacteria in bat flies

A heterozygous moth genome provides insights into herbivory and detoxification

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