Dataset Information

Primates, Lice and Bacteria: Speciation and Genome Evolution in the Symbionts of Hominid Lice.

ABSTRACT: Insects with restricted diets rely on symbiotic bacteria to provide essential metabolites missing in their diet. The blood-sucking lice are obligate, host-specific parasites of mammals and are themselves host to symbiotic bacteria. In human lice, these bacterial symbionts supply the lice with B-vitamins. Here, we sequenced the genomes of symbiotic and heritable bacterial of human, chimpanzee, gorilla, and monkey lice and used phylogenomics to investigate their evolutionary relationships. We find that these symbionts have a phylogenetic history reflecting the louse phylogeny, a finding contrary to previous reports of symbiont replacement. Examination of the highly reduced symbiont genomes (0.53-0.57?Mb) reveals much of the genomes are dedicated to vitamin synthesis. This is unchanged in the smallest symbiont genome and one that appears to have been reorganized. Specifically, symbionts from human lice, chimpanzee lice, and gorilla lice carry a small plasmid that encodes synthesis of vitamin B5, a vitamin critical to the bacteria-louse symbiosis. This plasmid is absent in an old world monkey louse symbiont, where this pathway is on its primary chromosome. This suggests the unique genomic configuration brought about by the plasmid is not essential for symbiosis, but once obtained, it has persisted for up to 25 My. We also find evidence that human, chimpanzee, and gorilla louse endosymbionts have lost a pathway for synthesis of vitamin B1, whereas the monkey louse symbiont has retained this pathway. It is unclear whether these changes are adaptive, but they may point to evolutionary responses of louse symbionts to shifts in primate biology.

SUBMITTER: Boyd BM

PROVIDER: S-EPMC5455983 | biostudies-literature | 2017 Jul

REPOSITORIES: biostudies-literature

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Publications

Primates, Lice and Bacteria: Speciation and Genome Evolution in the Symbionts of Hominid Lice.

Boyd Bret M BM Allen Julie M JM Nguyen Nam-Phuong NP Vachaspati Pranjal P Quicksall Zachary S ZS Warnow Tandy T Mugisha Lawrence L Johnson Kevin P KP Reed David L DL

Molecular biology and evolution 20170701 7

Insects with restricted diets rely on symbiotic bacteria to provide essential metabolites missing in their diet. The blood-sucking lice are obligate, host-specific parasites of mammals and are themselves host to symbiotic bacteria. In human lice, these bacterial symbionts supply the lice with B-vitamins. Here, we sequenced the genomes of symbiotic and heritable bacterial of human, chimpanzee, gorilla, and monkey lice and used phylogenomics to investigate their evolutionary relationships. We find ...[more]

PMID: 28419279

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Project description:BackgroundHost-symbiont co-speciation and reductive genome evolution have been commonly observed among obligate endocellular insect symbionts, while such examples have rarely been identified among extracellular ones, the only case reported being from gut symbiotic bacteria of stinkbugs of the family Plataspidae. Considering that gut symbiotic communities are vulnerable to invasion of foreign microbes, gut symbiotic associations have been thought to be evolutionarily not stable. Stinkbugs of the family Acanthosomatidae harbor a bacterial symbiont in the midgut crypts, the lumen of which is completely sealed off from the midgut main tract, thereby retaining the symbiont in the isolated cryptic cavities. We investigated histological, ecological, phylogenetic, and genomic aspects of the unique gut symbiosis of the acanthosomatid stinkbugs.ResultsPhylogenetic analyses showed that the acanthosomatid symbionts constitute a distinct clade in the gamma-Proteobacteria, whose sister groups are the obligate endocellular symbionts of aphids Buchnera and the obligate gut symbionts of plataspid stinkbugs Ishikawaella. In addition to the midgut crypts, the symbionts were located in a pair of peculiar lubricating organs associated with the female ovipositor, by which the symbionts are vertically transmitted via egg surface contamination. The symbionts were detected not from ovaries but from deposited eggs, and surface sterilization of eggs resulted in symbiont-free hatchlings. The symbiont-free insects suffered retarded growth, high mortality, and abnormal morphology, suggesting important biological roles of the symbiont for the host insects. The symbiont phylogeny was generally concordant with the host phylogeny, indicating host-symbiont co-speciation over evolutionary time despite the extracellular association. Meanwhile, some local host-symbiont phylogenetic discrepancies were found, suggesting occasional horizontal symbiont transfers across the host lineages. The symbionts exhibited AT-biased nucleotide composition, accelerated molecular evolution, and reduced genome size, as has been observed in obligate endocellular insect symbionts.ConclusionComprehensive studies of the acanthosomatid bacterial symbiosis provide new insights into the genomic evolution of extracellular symbiotic bacteria: host-symbiont co-speciation and drastic genome reduction can occur not only in endocellular symbiotic associations but also in extracellular ones. We suggest that many more such cases might be discovered in future surveys.

Project description:UNLABELLED: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.

Dataset Information

Primates, Lice and Bacteria: Speciation and Genome Evolution in the Symbionts of Hominid Lice.

Publications

Primates, Lice and Bacteria: Speciation and Genome Evolution in the Symbionts of Hominid Lice.

Similar Datasets

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