Comparative genomics of the emerging human pathogen Photorhabdus asymbiotica with the insect pathogen Photorhabdus luminescens

Paul Wilkinson,Isabella Vlisidou,Lisa Crossman,Louise Clark,Julian Parkhill,Mark Simmonds,David Harris,Nathalie Bason,Carol Churcher,Matthew Mayho,Alexandra Bignell,Andrew Barron,Craig Corton,Douglas Ormond,Nicholas R Waterfield ,Frances J.d Smith ,María Sánchez-Contreras ,Michael A Quail ,Nicholas Thompson ,Richard H Ffrench-Constant

doi:10.1186/1471-2164-10-302

Paul Wilkinson, Isabella Vlisidou + Show 18 more

Open Access

https://doi.org/10.1186/1471-2164-10-302

Copy DOI

Abstract

BackgroundThe Gram-negative bacterium Photorhabdus asymbiotica (Pa) has been recovered from human infections in both North America and Australia. Recently, Pa has been shown to have a nematode vector that can also infect insects, like its sister species the insect pathogen P. luminescens (Pl). To understand the relationship between pathogenicity to insects and humans in Photorhabdus we have sequenced the complete genome of Pa strain ATCC43949 from North America. This strain (formerly referred to as Xenorhabdus luminescens strain 2) was isolated in 1977 from the blood of an 80 year old female patient with endocarditis, in Maryland, USA. Here we compare the complete genome of Pa ATCC43949 with that of the previously sequenced insect pathogen P. luminescens strain TT01 which was isolated from its entomopathogenic nematode vector collected from soil in Trinidad and Tobago.ResultsWe found that the human pathogen Pa had a smaller genome (5,064,808 bp) than that of the insect pathogen Pl (5,688,987 bp) but that each pathogen carries approximately one megabase of DNA that is unique to each strain. The reduced size of the Pa genome is associated with a smaller diversity in insecticidal genes such as those encoding the Toxin complexes (Tc's), Makes caterpillars floppy (Mcf) toxins and the Photorhabdus Virulence Cassettes (PVCs). The Pa genome, however, also shows the addition of a plasmid related to pMT1 from Yersinia pestis and several novel pathogenicity islands including a novel Type Three Secretion System (TTSS) encoding island. Together these data suggest that Pa may show virulence against man via the acquisition of the pMT1-like plasmid and specific effectors, such as SopB, that promote its persistence inside human macrophages. Interestingly the loss of insecticidal genes in Pa is not reflected by a loss of pathogenicity towards insects.ConclusionOur results suggest that North American isolates of Pa have acquired virulence against man via the acquisition of a plasmid and specific virulence factors with similarity to those shown to play roles in pathogenicity against humans in other bacteria.

Highlights

The Gram-negative bacterium Photorhabdus asymbiotica (Pa) has been recovered from human infections in both North America and Australia
All of the Pa strains examined, either from North America or Australia, carry plasmids (Figure 1), whereas no other Photorhabdus strain we have examined from the two other main groups, P. luminescens (Pl) and P. temperata (Pt), shows the presence of any plasmid
BLAST analysis of pAU1 reveals few open reading frames predicting known proteins but reveals an extensive array of transposons similar to those found in the genome and plasmids of Y. pestis (Table 1) To date we have not been able to ascribe firm biological functions to the proteins predicted by pAU1 coding regions (CDs)

Summary

Introduction

The Gram-negative bacterium Photorhabdus asymbiotica (Pa) has been recovered from human infections in both North America and Australia. We compare the complete genome of Pa ATCC43949 with that of the previously sequenced insect pathogen P. luminescens strain TT01 which was isolated from its entomopathogenic nematode vector collected from soil in Trinidad and Tobago. We study the Photorhabdus group of bacteria which are associated with entomopathogenic nematodes (EPNs) and their insect hosts [4] Both the species P. luminescens (Pl) and P. temperata (Pt) have only ever been recovered from EPNs isolated from infected insect hosts. We have chosen to sequence the genome of one of the North American clinical isolates of P. asymbiotica strain ATCC43949 (formerly described as Xenorhabdus luminescens strain 2 [5]), in order to compare it with the previously sequenced insect pathogen P. luminescens TT01 recovered from its nematode vector, collected by baiting soil with insects, in Trinidad and Tobago. Recent comparative studies between the genome of Pl TT01 and Y. enterocolitica have highlighted the genes within Pl that are likely to be insecticidal [7], and here we identify genomic changes associated with the additional selective pressures exerted when Photorhabdus meets the vertebrate immune system for the first time

Methods

Results

Discussion

Conclusion