title: Metabolic Coevolution in the Bacterial Symbiosis of Whiteflies and Related Plant Sap-Feeding Insects.
abstract: Genomic decay is a common feature of intracellular bacteria that have entered into symbiosis with plant sap-feeding insects. This study of the whitefly Bemisia tabaci and two bacteria (Portiera aleyrodidarum and Hamiltonella defensa) cohoused in each host cell investigated whether the decay of Portiera metabolism genes is complemented by host and Hamiltonella genes, and compared the metabolic traits of the whitefly symbiosis with other sap-feeding insects (aphids, psyllids, and mealybugs). Parallel genomic and transcriptomic analysis revealed that the host genome contributes multiple metabolic reactions that complement or duplicate Portiera function, and that Hamiltonella may contribute multiple cofactors and one essential amino acid, lysine. Homologs of the Bemisia metabolism genes of insect origin have also been implicated in essential amino acid synthesis in other sap-feeding insect hosts, indicative of parallel coevolution of shared metabolic pathways across multiple symbioses. Further metabolism genes coded in the Bemisia genome are of bacterial origin, but phylogenetically distinct from Portiera, Hamiltonella and horizontally transferred genes identified in other sap-feeding insects. Overall, 75% of the metabolism genes of bacterial origin are functionally unique to one symbiosis, indicating that the evolutionary history of metabolic integration in these symbioses is strongly contingent on the pattern of horizontally acquired genes. Our analysis, further, shows that bacteria with genomic decay enable host acquisition of complex metabolic pathways by multiple independent horizontal gene transfers from exogenous bacteria. Specifically, each horizontally acquired gene can function with other genes in the pathway coded by the symbiont, while facilitating the decay of the symbiont gene coding the same reaction.
authors.affiliation: Department of Entomology, Cornell University.
authors.forename: Jun-Bo
authors.initials: JB
authors.lastname: Luan
authors.affiliation: Boyce Thompson Institute for Plant Research, Cornell University.
authors.forename: Wenbo
authors.initials: W
authors.lastname: Chen
authors.affiliation: Boyce Thompson Institute for Plant Research, Cornell University USDA-Agricultural Research Service, U.S. Vegetable Laboratory, Charleston, South Carolina.
authors.forename: Daniel K
authors.initials: DK
authors.lastname: Hasegawa
authors.affiliation: USDA-Agricultural Research Service, U.S. Vegetable Laboratory, Charleston, South Carolina.
authors.forename: Alvin M
authors.initials: AM
authors.lastname: Simmons
authors.affiliation: USDA-Agricultural Research Service, Crop Improvement and Protection Research, Salinas, California.
authors.forename: William M
authors.initials: WM
authors.lastname: Wintermantel
authors.affiliation: USDA-Agricultural Research Service, U.S. Vegetable Laboratory, Charleston, South Carolina.
authors.forename: Kai-Shu
authors.initials: KS
authors.lastname: Ling
authors.affiliation: Boyce Thompson Institute for Plant Research, Cornell University USDA-Agricultural Research Service, Robert W. Holley Center for Agriculture and Health, Ithaca, New York.
authors.forename: Zhangjun
authors.initials: Z
authors.lastname: Fei
authors.affiliation: Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, China shshliu@zhu.edu.cn aes326@cornell.edu.
authors.forename: Shu-Sheng
authors.initials: SS
authors.lastname: Liu
authors.affiliation: Department of Entomology, Cornell University Department of Molecular Biology and Genetics, Cornell University shshliu@zhu.edu.cn aes326@cornell.edu.
authors.forename: Angela E
authors.initials: AE
authors.lastname: Douglas
mesh_terms: D000818:Animals; D004755:Enterobacteriaceae / Q000235:genetics* / Q000378:metabolism; D019143:Evolution, Molecular; D020440:Gene Duplication; D049750:Genome, Insect; D044129:Halomonadaceae / Q000235:genetics* / Q000378:metabolism; D006430:Hemiptera / Q000235:genetics* / Q000378:metabolism / Q000382:microbiology*; D053858:Metabolic Networks and Pathways / Q000235:genetics; D013559:Symbiosis / Q000235:genetics*; D059467:Transcriptome
keywords: Bemisia tabaci; Hamiltonella; Portiera; amino acid biosynthesis; bacteriocyte; horizontal gene transfer