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Independent Origins of Vectored Plant Pathogenic Bacteria from Arthropod-Associated Arsenophonus Endosymbionts

  • Invertebrate Microbiology
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Abstract

The genus Arsenophonus (Gammaproteobacteria) is comprised of intracellular symbiotic bacteria that are widespread across the arthropods. These bacteria can significantly influence the ecology and life history of their hosts. For instance, Arsenophonus nasoniae causes an excess of females in the progeny of parasitoid wasps by selectively killing the male embryos. Other Arsenophonus bacteria have been suspected to protect insect hosts from parasitoid wasps or to expand the host plant range of phytophagous sap-sucking insects. In addition, a few reports have also documented some Arsenophonus bacteria as plant pathogens. The adaptation to a plant pathogenic lifestyle seems to be promoted by the infection of sap-sucking insects in the family Cixiidae, which then transmit these bacteria to plants during the feeding process. In this study, we define the specific localization of an Arsenophonus bacterium pathogenic to sugar beet and strawberry plants within the plant hosts and the insect vector, Pentastiridius leporinus (Hemiptera: Cixiidae), using fluorescence in situ hybridization assays. Phylogenetic analysis on 16S rRNA and nucleotide coding sequences, using both maximum likelihood and Bayesian criteria, revealed that this bacterium is not a sister taxon to “Candidatus Phlomobacter fragariae,” a previously characterized Arsenophonus bacterium pathogenic to strawberry plants in France and Japan. Ancestral state reconstruction analysis indicated that the adaptation to a plant pathogenic lifestyle likely evolved from an arthropod-associated lifestyle and showed that within the genus Arsenophonus, the plant pathogenic lifestyle arose independently at least twice. We also propose a novel Candidatus status, “Candidatus Arsenophonus phytopathogenicus” novel species, for the bacterium associated with sugar beet and strawberry diseases and transmitted by the planthopper P. leporinus.

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Acknowledgments

We are grateful to four anonymous reviewers for suggestions on the original version of the manuscript and to Elisabeth Boudon-Padieu at INRA Dijon for providing P. leporinus planthoppers and sugar beet plants used for the FISH assays. Research was supported by the University of Hawaii Start-up and Hatch funds to Alberto Bressan.

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Authors and Affiliations

  1. Department of Plant and Environmental Protection Sciences, University of Hawaii at Manoa, 3050 Maile Way, Honolulu, HI, 96822, USA

    Alberto Bressan

  2. Dipartimento di Scienze e Tecnologie Agroambientali-Patologia Vegetale, University of Bologna, Viale Fanin 40, 40127, Bologna, Italy

    Federica Terlizzi & Rino Credi

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  1. Alberto Bressan
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  2. Federica Terlizzi
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  3. Rino Credi
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Correspondence to Alberto Bressan.

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Figure S1

Results of fluorescence in situ hybridization assays on a thin section of Pentastiridius leporinus abdomen hybridized with both universal eubacterial probe, EUB338-Alexa Fluor488 (a) and SBR proteobacterium probe, SBR450-Texas Red (b). B 1 a bacteriome containing “Ca. Sulcia muelleri”-like cells, B 2 a bacteriome containing “Ca. Purcelliella pentastirinorum”-like cells and other large cells from an underscribed β-proteobacterium (***); Oo oocyte. Arrows indicate localization of SBR proteobacterium. Scale bars = 50 μm. (PDF 8457 kb)

Figure S2

Cladogram showing ancestral state reconstruction using parsimony analysis mapped onto 16S rRNA tree (PDF 642 kb)

Figure S3

Cladogram showing ancestral state reconstruction using parsimony analysis mapped onto spoT-spoU-recG tree. (PDF 603 kb)

Table S1

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Bressan, A., Terlizzi, F. & Credi, R. Independent Origins of Vectored Plant Pathogenic Bacteria from Arthropod-Associated Arsenophonus Endosymbionts. Microb Ecol 63, 628–638 (2012). https://doi.org/10.1007/s00248-011-9933-5

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