Competition and Co-existence of Two Photorhabdus Symbionts with a Nematode Host

Microb Ecol. 2021 Jan;81(1):223-239. doi: 10.1007/s00248-020-01573-y. Epub 2020 Aug 21.

Abstract

Photorhabdus spp. (Enterobacteriales: Morganellaceae) occur exclusively as symbionts of Heterorhabditis nematodes for which they provide numerous services, including killing insects and providing nutrition and defence within the cadavers. Unusually, two species (Photorhabdus cinerea and Photorhabdus temperata) associate with a single population of Heterorhabditis downesi at a dune grassland site. Building on previous work, we investigated competition between these two Photorhabdus species both at the regional (between insects) and local (within insect) level by trait comparison and co-culture experiments. There was no difference between the species with respect to supporting nematode reproduction and protection of cadavers against invertebrate scavengers, but P. cinerea was superior to P. temperata in several traits: faster growth rate, greater antibacterial and antifungal activity and colonisation of a higher proportion of nematodes in co-culture. Moreover, where both bacterial symbionts colonised single nematode infective juveniles, P. cinerea tended to dominate in numbers. Differences between Photorhabdus species were detected in the suite of secondary metabolites produced: P. temperata produced several compounds not produced by P. cinerea including anthraquinone pigments. Bioluminescence emitted by P. temperata also tended to be brighter than that from P. cinerea. Bioluminescence and pigmentation may protect cadavers against scavengers that rely on sight. We conclude that while P. cinerea may show greater local level (within-cadaver) competitive success, co-existence of the two Photorhabdus species in the spatially heterogeneous environment of the dunes is favoured by differing specialisations in defence of the cadaver against differing locally important threats.

Keywords: Bioluminescence; Entomopathogenic nematode; Niche separation; Scavenger deterrence; Secondary metabolites; Symbiosis.

MeSH terms

  • Animals
  • Anthraquinones / metabolism
  • Grassland
  • Luminescent Measurements
  • Photorhabdus / growth & development
  • Photorhabdus / metabolism*
  • Secondary Metabolism / physiology
  • Strongyloidea / microbiology*
  • Symbiosis / physiology*

Substances

  • Anthraquinones

Supplementary concepts

  • Photorhabdus cinerea
  • Photorhabdus temperata