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PMID: 17032065 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Strict host-symbiont cospeciation and reductive genome evolution in insect gut bacteria.

PLoS biology ·Vol. 4 ·No. 10 ·2006-10-00 ·Pages e337

Hosokawa T, Kikuchi Y, Nikoh N, Shimada M, Fukatsu T

Abstract

Host-symbiont cospeciation and reductive genome evolution have been identified in obligate endocellular insect symbionts, but no such example has been identified from extracellular ones. Here we first report such a case in stinkbugs of the family Plataspidae, wherein a specific gut bacterium is vertically transmitted via "symbiont capsule." In all of the plataspid species, females produced symbiont capsules upon oviposition and their gut exhibited specialized traits for capsule production. Phylogenetic analysis showed that the plataspid symbionts constituted a distinct group in the gamma-Proteobacteria, whose sister group was the aphid obligate endocellular symbionts Buchnera. Removal of the symbionts resulted in retarded growth, mortality, and sterility of the insects. The host phylogeny perfectly agreed with the symbiont phylogeny, indicating strict host-symbiont cospeciation despite the extracellular association. The symbionts exhibited AT-biased nucleotide composition, accelerated molecular evolution, and reduced genome size, as has been observed in obligate endocellular insect symbionts. These findings suggest that not the endocellular conditions themselves but the population genetic attributes of the vertically transmitted symbionts are probably responsible for the peculiar genetic traits of these insect symbionts. We proposed the designation "Candidatus Ishikawaella capsulata" for the plataspid symbionts. The plataspid stinkbugs, wherein the host-symbiont associations can be easily manipulated, provide a novel system that enables experimental approaches to previously untouched aspects of the insect-microbe mutualism. Furthermore, comparative analyses of the sister groups, the endocellular Buchnera and the extracellular Ishikawaella, would lead to insights into how the different symbiotic lifestyles have affected their genomic evolution.

MeSH Terms
Animals Buchnera/genetics,physiology Evolution, Molecular Female Gastrointestinal Tract/microbiology Genome, Bacterial Heteroptera/genetics,microbiology Host-Parasite Interactions/genetics Molecular Sequence Data Phylogeny Symbiosis
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Hosokawa Takahiro
Institute for Biological Resources and Functions, National Institute of Advanced Industrial Science and Technology, Tsukuba, Japan.
Kikuchi Yoshitomo
Nikoh Naruo
Shimada Masakazu
Fukatsu Takema
Conflict of Interest

Competing interests. The authors have declared that no competing interests exist.

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Article Info
Journal
PLoS biology
Abbr.
PLoS Biol
ISSN
1545-7885
DOI
10.1371/journal.pbio.0040337
Published
2006-10-00
Pages
e337
Language
English
Region
United States
NLM ID
101183755
PMCID
PMC1592312
Subset
IM
Databases
GENBANK
AB013086, AB030020, AB037545, AB063521, AB240157, AB240158, AB240159, AB240160, AB240161, AB240162, AB240163, AB240164, AB240165, AB240166, AB240167, AB240168, AB240169, AB240170, AB240572, AB240573, AB240574, AB240576, AB244765, AB244766, AB244767, AB244768, AB244769, AE013602, AF005235, AF013087, AF124042, AF293616, AF293618, AF465793, AJ007404, AJ296751, AP008232, AY126635, D14555, DQ115536, J01695, M27039, M27040, U88545, X07714, X74694, Z11925
Corrections
CommentIn
PMID: 20076479
External Links
PubMed source DOI: 10.1371/journal.pbio.0040337 PMC Full Text View journal details
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