Whole-genome-based revisit of Photorhabdus phylogeny: proposal for the elevation of most Photorhabdus subspecies to the species level and description of one novel species Photorhabdus bodei sp. nov., and one novel subspecies Photorhabdus laumondii subsp. clarkei subsp. nov.

Machado, Ricardo A. R.; Wüthrich, Daniel; Kuhnert, Peter; Arce, Carla C. M.; Thönen, Lisa; Ruiz, Celia; Zhang, Xi; Robert, Christelle; Karimi, Javad; Kamali, Shokoofeh; Ma, Jingyun; Bruggmann, Rémy; Erb, Matthias

doi:10.1099/ijsem.0.002820

Cited by 138 publications

(69 citation statements)

References 74 publications

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“…To test whether the EPN endosymbiontic bacterium Photorhabdus laumondii subsp. laumondii (28) may be responsible for BHT production, we injected it into WCR larvae directly, which resulted in visual infection symptoms and mortality similar to EPN infection. No BHT release from P. laumondii infected WCR cadavers was detected (Fig.…”

Section: Resultsmentioning

confidence: 99%

Entomopathogenic nematodes increase predation success by inducing specific cadaver volatiles that attract healthy herbivores

Zhang

Machado

Doan

et al. 2018

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14Herbivore natural enemies, including predators, parasitoids and parasites, protect plants by 15 regulating herbivore populations. Some parasites can increase their transmission efficiency by 16 manipulating host behavior. Whether natural enemies can manipulate herbivore behavior to 17 increase top-down control, however, is unknown. Here, we investigate if and how the 18 entomopathogenic nematode Heterorhabditis bacteriophora, an important biocontrol agent, 19 modulates the behavior of the western corn rootworm, Diabrotica virgifera virgifera, a major 20 maize pest, and how these behavioral changes affect the capacity of the nematode to control the 21 rootworm. We found that healthy rootworm larvae are attracted to nematode-infected cadavers 22 shortly before the emergence of the next generation of nematodes. Nematode-infected rootworms 23 release distinct volatile bouquets, including butylated hydroxytoluene (BHT), which attracts 24 rootworms to infected cadavers. In a soil setting, BHT attracts rootworms and reduces nematode 25 resistance, resulting in increased infection rates and rootworm mortality as well as increased 26 nematode reproductive success. Five out of seven tested insect species were found to be attracted 27 to nematode-infected conspecifics, suggesting that attraction of healthy hosts to nematode-infected 28 cadavers is widespread. This study reveals a new facet of the biology of entomopathogenic 29 nematodes that increases their capacity to control a major root pest by increasing the probability of 30 host encounters. 31 Keywords: Belowground tritrophic interactions, entomopathogenic nematodes, prey attraction, 32 parasitism strategies, butylated hydroxytoluene 33 34Herbivore natural enemies such as predators, parasites and parasitoids play a key role in terrestrial 35 ecosystems by reducing herbivore abundance (1). Biological control relies on this form of top-36 down control to protect crops from herbivores (2). In order to exert their effects, herbivore natural 37 enemies need to make contact with their hosts. Natural enemies have evolved various behavioral 38 strategies to maximize their chance to encounter herbivores (3-6). Predators and parasitoids for 39 instance can use herbivore-induced plant volatiles to locate herbivores (7). Herbivores on the other 40 hand can detect and actively avoid contact with natural enemies (8). The interplay between 41 behavioral adaptations of herbivores and natural enemies is likely to be an important determinant 42 for the success of herbivore natural enemies and their capacity to suppress herbivore pests. 43A key step in the life of many herbivore natural enemies is the acquisition of new hosts once the 44 old host is exploited. Predators and parasitoids acquire new hosts by hunting, ambushing and 45 trapping them. Parasites with indirect life cycles can also facilitate the transfer to new hosts through 46 host manipulation strategies, including changes in color, smell and behavior of their current hosts 47 to attract alternate hosts (9-12). How p...

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Section: Resultsmentioning

confidence: 99%

Entomopathogenic nematodes increase predation success by inducing specific cadaver volatiles that attract healthy herbivores

Zhang

Machado

Doan

et al. 2018

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“…Five to ten days later, all nematode-infected G. mellonella larvae were individually transferred to white traps (56), and emerging nematodes were used to infect another set of G. mellonella larvae (57). Irrespective of whether they were isolated from the field or obtained from collaborators, all nematodes were identified by internal transcribed spacer rRNA gene sequencing as described previously (58-60). The collected nematode progeny was maintained in 250 ml flasks (Greiner Bio-One GmbH, Frickenhausen, DE) at a density of one EPN per microliter tap water at 10 °C.…”

Section: Methodsmentioning

confidence: 99%

Plant defense resistance in natural enemies of a specialist insect herbivore

Zhang

Doan

Arce

et al. 2019

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25 42 the improvement of biological control agents. 43 44 Key words: Tritrophic interactions, plant secondary metabolism, biological control. 45 101Nematode strains from other parts of the world never encountered the western corn rootworm, as 102 they came from regions where the rootworm is not present, or they were isolated before the western 103 corn rootworm invaded these regions (table S1). 104 Using internal transcribed spacer rRNA gene sequencing, 19 nematode strains within our 105 collection were confirmed to be H. bacteriophora. Three strains from China were re-classified as 106 H. beicheriana, and three strains from the US were identified as H. georgiana, both of which are 107 closely related to H. bacteriophora. In a first experiment, we compared the infectiveness of the 108 different nematode strains towards larvae of the western corn rootworm and larvae of the banded 109 5 cucumber beetle (D. balteata). In contrast to the western corn rootworm, the banded cucumber 110 beetle feeds on many different plant species apart from maize and does not sequester 111 benzoxazinoids ( Fig. 1B and S1) (28). The banded cucumber beetle occurs mainly in Central 112 America, Mexico and the Southern US, outside of our collection range. Thus, none of the tested 113 Infectivity tests revealed a significant interaction between the host herbivore species and the 129 evolutionary history of the nematodes (Fig. 1C, table S3). Nematode strains from the primary range 130 of the western corn rootworm were able to infect and kill the western corn rootworm and the 131 banded cucumber equally well. By contrast, the infectivity of nematodes from outside the primary 132 157 418 strains,

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“…al. (41,42). Briefly, Bacterial genomic DNA was extracted using the GenElute Bacterial Genomic DNA Kit (Sigma-Aldrich) following the manufacturer's instructions.…”

Section: Generation Of Phylogenetic Treesmentioning

confidence: 99%

“…Due to their importance as biocontrol agents, human pathogens, and bio-factories, substantial efforts have been made to understand the diversity of the Photorhabdus bacterial group. For this, several collection campaigns have been set around the world which have yield many different isolates (30)(31)(32)(33)(34)(35)(36)(37)(38)(39)(40)(41)(42)(43).…”

Section: Introductionmentioning

confidence: 99%

“…Later, multi locus sequence analysis (MLSA) was found to be a useful tool for the taxonomic description of Photorhabdus species (49). However, with an increasing number of available strains and due to the high taxonomic complexity of this bacterial group, whole-genome based methods were shown to be particularly suitable to resolve the phylogenetic relationship of especially closely related Photorhabdus species and subspecies (41,42). Nonetheless, these methods are laborious and do not allow for a rapid identification.…”

Section: Introductionmentioning

confidence: 99%

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Identification ofPhotorhabdussymbionts by MALDI-TOF mass spectrometry

Hill

Kuhnert

Erb

et al. 2020

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Species of the bacterial genus Photorhabus live in a symbiotic relationship with Heterorhabditis entomopathogenic nematodes. Besides their use as biological control agents against agricultural pests, some Photorhabdus species are also a source of natural products and are of medical interest due to their ability to cause tissue infections and subcutaneous lesions in humans. Given the diversity of Photorhabdus species, rapid and reliable methods to resolve this genus to the species level are needed.In this study, we evaluated the potential of matrix-assisted laser desorption/ionization time-of flight mass spectrometry (MALDI-TOF MS) for the identification of Photorhabdus species. To this end, we established a collection of 55 isolates consisting of type strains and multiple field strains that belong to each of the validly described species and subspecies of this genus. Reference spectra for the strains were generated and used to complement a currently available database. The extended reference database was then used for identification based on the direct transfer and protein fingerprint of single colonies. High discrimination of distantly related species was observed. However, lower discrimination was observed with some of the most closely related species and subspecies. Our results, therefore, suggest that MALDI-TOF MS can be used to correctly identify Photorhabdus strains at the genus and species level, but has limited resolution power for closely related species and subspecies. Our study demonstrates the suitability and limitations of MALDI-TOF-based identification methods for the assessment of the taxonomical position and identification of Photorhabdus isolates. Impact StatementSpecies of the bacterial genus Photorhabus live in close association with soil-born entomopathogenic nematodes. Under natural conditions, these bacteria are often observed infecting soil-associated arthropods, but under certain circumstances, can also infect humans. They produce a large variety of natural products including antibiotics, insecticides, and polyketid pigments that have substantial agricultural, biotechnological and medical potential. In this study, we implement a MALDI-TOF MSbased identification method to resolve the taxonomic identity of this bacterial genus, providing thereby a rapid identification tool to understanding its taxonomic diversity to boost scientific progress in medical, agricultural, and biotechnological settings.

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Whole-genome-based revisit of Photorhabdus phylogeny: proposal for the elevation of most Photorhabdus subspecies to the species level and description of one novel species Photorhabdus bodei sp. nov., and one novel subspecies Photorhabdus laumondii subsp. clarkei subsp. nov.

Cited by 138 publications

References 74 publications

Entomopathogenic nematodes increase predation success by inducing specific cadaver volatiles that attract healthy herbivores

Entomopathogenic nematodes increase predation success by inducing specific cadaver volatiles that attract healthy herbivores

Plant defense resistance in natural enemies of a specialist insect herbivore

Identification ofPhotorhabdussymbionts by MALDI-TOF mass spectrometry

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