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Front. Microbiol. | doi: 10.3389/fmicb.2018.02254

To B or not to B: comparative genomics suggests Arsenophonus as a source of B vitamins in whiteflies

  • 1Department of Entomology, Faculty of Agriculture, Food and Environment, Hebrew University of Jerusalem, Israel
  • 2Institute of Plant Sciences, Newe Ya'ar Research Center, Agricultural Research Organization, Volcani Center, Israel
  • 3Department of Entomology, Newe Ya'ar Research Center, Agricultural Research Organization, Volcani Center, Israel
  • 4Instituto de Biología Integrativa de Sistemas (I2SysBio), Spain
  • 5Unidad Mixta de Investigación en Genómica y Salud, Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana (FISABIO), Spain

Insect lineages feeding on nutritionally restricted diets such as phloem sap, xylem sap, or blood, were able to diversify by acquiring bacterial species that complement lacking nutrients. These bacteria, considered obligate/primary endosymbionts, share a long evolutionary history with their hosts. In some cases, however, these endosymbionts are not able to fulfill all of their host’s nutritional requirements, driving the acquisition of additional symbiotic species. Phloem-feeding members of the insect family Aleyrodidae (whiteflies) established an obligate relationship with Candidatus Portiera aleyrodidarum, which provides its hots with essential amino acids and carotenoids. In addition, many whitefly species harbor additional endosymbionts which may potentially further supplement their host’s diet. To test this hypothesis, genomes of several endosymbionts of the whiteflies Aleurodicus dispersus, Aleurodicus floccissimus and Trialeurodes vaporariorum were analyzed. In addition to Portiera, all three species were found to harbor one Arsenophonus and one Wolbachia endosymbiont. A comparative analysis of Arsenophonus genomes revealed that although all three are capable of synthesizing B vitamins and cofactors, such as pyridoxal, riboflavin, or folate, their genomes and phylogenetic relationship vary greatly. Arsenophonus of A. floccissimus and T. vaporariorum belong to the same clade, and display characteristics of facultative endosymbionts, such as large genomes (3 Mb) with thousands of genes and pseudogenes, intermediate GC content, and mobile genetic elements. In contrast, Arsenophonus of A. dispersus belongs to a different lineage and displays the characteristics of a primary endosymbiont – a reduced genome (670 kb) with ~400 genes, 32% GC content, and no mobile genetic elements. However, the presence of 274 pseudogenes suggests that this symbiotic association is more recent than other reported primary endosymbionts of hemipterans. The gene repertoire of Arsenophonus of A. dispersus is completely integrated in the symbiotic consortia, and the biosynthesis of most vitamins occurs in shared pathways with its host. In addition, Wolbachia endosymbionts have also retained the ability to produce riboflavin, flavin adenine dinucleotide, and folate, and may make a nutritional contribution. Taken together, our results show that Arsenophonus hold a pivotal place in whitefly nutrition by their ability to produce B vitamins.

Keywords: whitefly, Symbiosis, Vitamins, Genome Reduction, Arsenophonus, Wolbachia, Metabolic complementation, Riboflavin

Received: 23 May 2018; Accepted: 04 Sep 2018.

Edited by:

Martin G. Klotz, Washington State University, United States

Reviewed by:

David Baltrus, University of Arizona, United States
Piotr Lukasik, University of Montana, United States  

Copyright: © 2018 Santos-Garcia, Juravel, Freilich, Zchori-Fein, Latorre, Moya, Morin and Silva. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence:
Dr. Diego Santos-Garcia, Faculty of Agriculture, Food and Environment, Hebrew University of Jerusalem, Department of Entomology, Rehovot, Israel, diego.santos@mail.huji.ac.il
Prof. Francisco J. Silva, Instituto de Biología Integrativa de Sistemas (I2SysBio), Paterna, Spain, francisco.silva@uv.es