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An Entomopathogenic Nematode Extends Its Niche by Associating with Different Symbionts

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Abstract

Bacterial symbionts are increasingly recognised as mediators of ecologically important traits of their animal hosts, with acquisition of new traits possible by uptake of novel symbionts. The entomopathogenic nematode Heterorhabditis downesi associates with two bacterial symbionts, Photorhabdus temperata subsp. temperata and P. temperata subsp. cinerea. At one intensively studied coastal dune site, P. temperata subsp. cinerea is consistently more frequently isolated than P. temperata subsp. temperata in H. downesi recovered from under the bare sand/Ammophila arrenaria of the front dunes (where harsh conditions, including drought, prevail). This is not the case in the more permissive closed dune grassland further from the sea. No differences were detected in ITS1 (internal transcribed spacer) sequence between nematode lines carrying either of the two symbiont subspecies, nor did they differ in their ability to utilise insects from three orders. The two symbionts could be readily swapped between lines, and both were carried in equal numbers within infective juveniles. In laboratory experiments, we tested whether the symbionts differentially affected nematode survival in insect cadavers that were allowed to dry. We assessed numbers of nematode infective juveniles emerging from insects that had been infected with H. downesi carrying either symbiont subspecies and then allowed to desiccate for up to 62 days. In moist conditions, cadavers produced similar numbers of nematodes, irrespective of the symbiont subspecies present, while under desiccating conditions, P. temperata subsp. cinerea cadavers yielded more nematode progeny than P. temperata subsp. temperata cadavers. Desiccating cadavers with the same nematode isolates, carrying either one or the other symbiont subspecies, confirmed that the symbiont was responsible for differences in nematode survival. Moreover, cadavers harbouring P. temperata subsp. cinerea had a reduced rate of drying relative to cadavers harbouring P. temperata subsp. temperata. Our experiments support the hypothesis that H. downesi can extend its niche into harsher conditions by associating with P. temperata subsp. cinerea.

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Acknowledgments

A.M.D. Maher was funded by a doctoral fellowship from the Irish Research Council for Science, Engineering and Technology (IRCSET); M. Asaiyah was funded by a Postgraduate Scholarship from the Ministry of Higher Education and Scientific Research in Lybia. We are grateful to Dr. David Fitzpatrick for advice on bioinformatics and to Prof. M.J. Downes and the anonymous referees for their helpful comments on the manuscript.

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Authors and Affiliations

  1. Department of Biology, Maynooth University, Maynooth, County Kildare, Ireland

    Abigail M. D. Maher, Mohamed A. M. Asaiyah & Christine T. Griffin

  2. Department of Mathematics and Statistics, Maynooth University, Maynooth, County Kildare, Ireland

    Caroline Brophy

  3. Department of Biology, Azzaytuna University, Tarhouna, Libya

    Mohamed A. M. Asaiyah

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  1. Abigail M. D. Maher
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Correspondence to Christine T. Griffin.

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Sequences

GenBank accession numbers for Heterorhabditis downesi: KU573057, KU573058, KU573059, KU573060, KU573061, KU573062

Photorhabdus temperata subspecies temperata: KU559326, KU559327, KU559328

Photorhabdus temperata subspecies cinerea: KU559323, KU559324, KU559325

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Maher, A.M.D., Asaiyah, M.A.M., Brophy, C. et al. An Entomopathogenic Nematode Extends Its Niche by Associating with Different Symbionts. Microb Ecol 73, 211–223 (2017). https://doi.org/10.1007/s00248-016-0829-2

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