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Phenotypic and Genomic Comparison of Photorhabdus Luminescens Subsp

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Phenotypic and Genomic Comparison of Photorhabdus Luminescens Subsp Zamora-Lagos et al. BMC Genomics (2018) 19:854 https://doi.org/10.1186/s12864-018-5121-z RESEARCH ARTICLE Open Access Phenotypic and genomic comparison of Photorhabdus luminescens subsp. laumondii TT01 and a widely used rifampicin-resistant Photorhabdus luminescens laboratory strain Maria-Antonia Zamora-Lagos1†, Simone Eckstein2†, Angela Langer2, Athanasios Gazanis2, Friedhelm Pfeiffer1 , Bianca Habermann1,3* and Ralf Heermann2* Abstract Background: Photorhabdus luminescens is an enteric bacterium, which lives in mutualistic association with soil nematodes and is highly pathogenic for a broad spectrum of insects. A complete genome sequence for the type strain P. luminescens subsp. laumondii TT01, which was originally isolated in Trinidad and Tobago, has been described earlier. Subsequently, a rifampicin resistant P. luminescens strain has been generated with superior possibilities for experimental characterization. This strain, which is widely used in research, was described as a spontaneous rifampicin resistant mutant of TT01 and is known as TT01-RifR. Results: Unexpectedly, upon phenotypic comparison between the rifampicin resistant strain and its presumed parent TT01, major differences were found with respect to bioluminescence, pigmentation, biofilm formation, haemolysis as well as growth. Therefore, we renamed the strain TT01-RifR to DJC. To unravel the genomic basis of the observed differences, we generated a complete genome sequence for strain DJC using the PacBio long read technology. As strain DJC was supposed to be a spontaneous mutant, only few sequence differences were expected. In order to distinguish these from potential sequencing errors in the published TT01 genome, we re-sequenced a derivative of strain TT01 in parallel, also using the PacBio technology. The two TT01 genomes differed at only 30 positions. In contrast, the genome of strain DJC varied extensively from TT01, showing 13,000 point mutations, 330 frameshifts, and 220 strain-specific regions with a total length of more than 300 kb in each of the compared genomes. Conclusions: According to the major phenotypic and genotypic differences, the rifampicin resistant P. luminescens strain, now named strain DJC, has to be considered as an independent isolate rather than a derivative of strain TT01. Strains TT01 and DJC both belong to P. luminescens subsp. laumondii. Background two species are highly pathogenic toward insects, P. asym- Photorhabdus spp. are pathogenic enteric bacteria that biotica is additionally associated with severe soft-tissue and maintain a mutualistic interaction with heterorhabditid systemic infections in humans, and is considered as an nematodes and can infect a wide variety of insect species. emerging threat [2]. Commonly, the bacteria colonize the To date, three Photorhabdus species are known: P. lumines- gut of the infective juvenile stage of Heterorhabditis spp. cens, P. temperata,andP. asymbiotica [1]. Whereas the first nematodes. Upon entering insect larvae, the nematodes in- ject the bacteria by regurgitation into the insect’s hemocoel. * Correspondence: [email protected]; [email protected] † Onceinsidetheinsect,thebacteriareplicaterapidlyand Maria-Antonia Zamora-Lagos and Simone Eckstein contributed equally to quickly establish a lethal septicaemia in the host by produc- this work. 1Computational Biology Group, Max-Planck-Institute of Biochemistry, Am tion of a broad range of different toxins that kill the insect Klopferspitz 18, 82152 Martinsried, Germany within 48 h. Bioconversion of the insect’s body by Photo- 2 Biozentrum, Bereich Mikrobiologie, Ludwig-Maximilians-Universität rhabdus spp. produces a rich food source for the bacteria as München, Großhaderner Str. 2-4, 82152 Martinsried, Germany Full list of author information is available at the end of the article well as for the nematodes. Nematode reproduction is © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Zamora-Lagos et al. BMC Genomics (2018) 19:854 Page 2 of 17 supported by the bacteria, probably by providing essential one inoculated with strain DJC turned orange, revealing nutrients that are required for efficient nematode prolifera- that both P. luminescens strains have differences in sec- tion [3]. Furthermore, the bacteria produce several second- ondary metabolite production and/or the regulation of ary metabolites like antibiotics to defend the insect cadaver the corresponding genes (Fig. 1b). from invasion by other microorganisms. P. luminescens Pathogenicity and bioluminescence. We next analyzed glows because of bacterial luciferase production. When the pathogenicity against Galleria mellonella wax moth larvae insect cadaver is depleted, the nematodes and bacteria of both P. luminescens strains. For that purpose, G. mello- re-associate and emerge from the carcass in search for a nella larvae were infected with either 200 or 200,000 cells, newinsecthost(see[4, 5]forreview). respectively, of P. luminescens strain TT01 or DJC. How- P. luminescens subsp. laumondii strain TT01 (DSM ever, we could not observe major differences in pathogen- 15139) was originally isolated from Heterorhabditis bac- icity between the two strains: 100% of the larvae died teriophora nematodes in Trinidad and Tobago [6]. Since within 48 h after infection either with strain TT01 or DJC, strain TT01 was difficult to access for genetic manipula- respectively. Approximately 1/3 of the larvae even died tion methods, a rifampicin resistant strain was isolated after 24 h for both strains at the higher bacterial load (Fig. by the group of David J. Clarke (University College Cork, 1c). Furthermore, G. mellonella larvae killed by either Ireland) by growing strain TT01 in the presence of the TT01 or DJC both turned red due to anthraquinone pro- antibiotic [7]. This strain showed enhanced suitability duction and were both positive for bioluminescence (Fig. for genetic manipulation due to the resistance marker, 1c). Additionally, light production of populations of both and was described as a spontaneous rifampicin resistant strains was quantified in liquid culture. Here we observed mutant of strain TT01 (TT01-RifR)[7]. In the scientific that bioluminescence of P. luminescens strain TT01 was literature, authors working with either TT01-RifR or the significantly higher compared to strain DJC (p-value < original TT01 strain commonly refer only to TT01, 0.001), especially at the time point of growth when the making this assignment highly ambiguous [8–10]. cells entered the stationary growth phase (Fig. 1d). Here we performed a phenotypic comparison between Nematode symbiosis. To investigate the symbiotic cap- P. luminescens strains TT01 and TT01-RifR. Since both acity of both P. luminescens strains, we tested whether strains differed in many phenotypic traits, we performed the bacteria were able to support nematode develop- detailed genomic analysis, generating a finalized complete ment. For that purpose, infective juveniles (IJs) of Het- genome sequence based on the PacBio long read approach erorhabditis bacteriophora were added to lipid agar [11]. We compared the genomes of the two strains in de- plates containing either P. luminescens strain TT01 or tail and report extensive sequence differences, indicating DJC, respectively. After 8 days of incubation, the num- that TT01-RifR is an independent isolate from type strain ber of hermaphrodites that developed from the IJs were TT01. Therefore, we renamed TT01-RifR to DJC. counted. No significant differences between P. lumines- cens strain TT01 and DJC were observed (Fig. 1e). Results Rifampicin resistance. Strains DJC and TT01 were tested Phenotypic comparison of P. luminescens strains TT01 and for rifampicin resistance, and only strain DJC was found to DJC be resistant (Fig. 2a). Furthermore, we tested both strains As a first step to investigate the differences between P. for their ability to produce exoproteinases, their ability to luminescens TT01 and DJC we started by comparing perform haemolysis and for antibiotic production (Fig. 2a). some of the most important phenotypes of Photorhab- To compare proteolytic activity, we spotted P. luminescens dus spp. like growth rate, pigmentation, biolumines- strain TT01 and DJC, respectively, on Ca-caseinate agar cence, insect pathogenicity and nematode support. plates. Both strains showed comparable protein degradation Growth behaviour. P. luminescens strains TT01 and (Fig. 2a). Furthermore, we plated both strains on sheep DJC showed differences in growth behaviour. The blood agar plates and LB agar plates to investigate haemoly- growth rate in the exponential growth phase was higher sis and antibiotic production, respectively. Surprisingly, P. for strain TT01 (μ = 0.39/h) compared to DJC (μ = 0.16/ luminescens DJC showed a significantly higher haemolytic h). Furthermore, in LB broth strain TT01 (OD600 = 21) activity (p-value < 0.001) as well as antibiotic production reached higher cell densities compared to strain DJC (p-value < 0.05) compared
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