Isolation and identification of Xenorhabdus and Photorhabdus bacteria associated with entomopathogenic nematodes and their larvicidal activity against Aedes aegypti

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Abstract

Background

Aedes aegypti is a potential vector of West Nile, Japanese encephalitis, chikungunya, dengue and Zika viruses. Alternative control measurements of the vector are needed to overcome the problems of environmental contamination and chemical resistance. Xenorhabdus and Photorhabdus are symbionts in the intestine of entomopathogenic nematodes (EPNs) Steinernema spp. and Heterorhabditis spp. These bacteria are able to produce a broad range of bioactive compounds including antimicrobial, antiparasitic, cytotoxic and insecticidal compounds. The objectives of this study were to identify Xenorhabdus and Photorhabdus isolated from EPNs in upper northern Thailand and to study their larvicidal activity against Ae. aegypti larvae.

Results

A total of 60 isolates of symbiotic bacteria isolated from EPNs consisted of Xenorhabdus (32 isolates) and Photorhabdus (28 isolates). Based on recA gene sequencing, BLASTN and phylogenetic analysis, 27 isolates of Xenorhabdus were identical and closely related to X. stockiae, 4 isolates were identical to X. miraniensis, and one isolate was identical to X. ehlersii. Twenty-seven isolates of Photorhabdus were closely related to P. luminescens akhurstii and P. luminescens hainanensis, and only one isolate was identical and closely related to P. luminescens laumondii. Xenorhabdus and Photorhabdus were lethal to Ae aegypti larvae. Xenorhabdus ehlersii bMH9.2_TH showed 100% efficiency for killing larvae of both fed and unfed conditions, the highest for control of Ae. aegypti larvae and X. stockiae (bLPA18.4_TH) was likely to be effective in killing Ae. aegypti larvae given the mortality rates above 60% at 72 h and 96 h.

Conclusions

The common species in the study area are X. stockiae, P. luminescens akhurstii, and P. luminescens hainanensis. Three symbiotic associations identified included P. luminescens akhurstii-H. gerrardi, P. luminescens hainanensis-H. gerrardi and X. ehlersii-S. Scarabaei which are new observations of importance to our knowledge of the biodiversity of, and relationships between, EPNs and their symbiotic bacteria. Based on the biological assay, X. ehlersii bMH9.2_TH begins to kill Ae. aegypti larvae within 48 h and has the most potential as a pathogen to the larvae. These data indicate that X. ehlersii may be an alternative biological control agent for Ae. aegypti and other mosquitoes.

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Most cited references 44

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Globalization, land use, and the invasion of West Nile virus.

A. Kilpatrick (2011)

Many invasive species that have been spread through the globalization of trade and travel are pathogens. A paradigmatic case is the introduction of West Nile virus (WNV) into North America in 1999. A decade of research on the ecology and evolution of WNV includes three findings that provide insight into the outcome of future pathogen introductions. First, WNV transmission in North America is highest in urbanized and agricultural habitats, in part because the hosts and vectors of WNV are abundant in human-modified areas. Second, after its introduction, the virus quickly adapted to infect local mosquito vectors more efficiently than the originally introduced strain. Third, highly focused feeding patterns of the mosquito vectors of WNV result in unexpected host species being important for transmission. This research provides a framework for predicting and preventing the emergence of foreign vector-borne pathogens.

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Declining malaria, rising of dengue and Zika virus: insights for mosquito vector control.

Giovanni Benelli, Heinz Mehlhorn (2016)

The fight against mosquito-borne diseases is a challenge of huge public health importance. To our mind, 2015 was an extraordinary year for malaria control, due to three hot news: the Nobel Prize to Youyou Tu for the discovery of artemisinin, the development of the first vaccine against Plasmodium falciparum malaria [i.e. RTS,S/AS01 (RTS,S)], and the fall of malaria infection rates worldwide, with special reference to sub-Saharan Africa. However, there are major challenges that still deserve attention, in order to boost malaria prevention and control. Indeed, parasite strains resistant to artemisinin have been detected, and RTS,S vaccine does not offer protection against Plasmodium vivax malaria, which predominates in many countries outside of Africa. Furthermore, the recent outbreaks of Zika virus infections, occurring in South America, Central America and the Caribbean, represent the most recent of four arrivals of important arboviruses in the Western Hemisphere, over the last 20 years. Zika virus follows dengue (which slyly arrived in the hemisphere over decades and became more aggressive in the 1990s), West Nile virus (emerged in 1999) and chikungunya (emerged in 2013). Notably, there are no specific treatments for these arboviruses. The emerging scenario highlights that the effective and eco-friendly control of mosquito vectors, with special reference to highly invasive species such as Aedes aegypti and Aedes albopictus, is crucial. The concrete potential of screening plant species as sources of metabolites for parasitological purposes is worthy of attention, as elucidated by the Y. Tu's example. Notably, plant-borne molecules are often effective at few parts per million against Aedes, Ochlerotatus, Anopheles and Culex young instars, can be used for the rapid synthesis of mosquitocidal nanoformulations and even employed to prepare cheap repellents with low human toxicity. In addition, behaviour-based control tools relying to the employ of sound traps and the manipulation of swarming behaviour (i.e. "lure and kill" approach) are discussed. The importance of further research on the chemical cues routing mosquito swarming and mating dynamics is highlighted. Besides radiation, transgenic and symbiont-based mosquito control approaches, an effective option may be the employ of biological control agents of mosquito young instars, in the presence of ultra-low quantities of nanoformulated botanicals, which boost their predation rates.

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Xenorhabdus and Photorhabdus spp.: bugs that kill bugs.

S Forst, B C Dowds, N Boemare … (1997)

Xenorhabdus and Photorhabdus spp. are gram negative gamma proteobacteria that form entomopathogenic symbioses with soil nematodes. They undergo a complex life cycle that involves a symbiotic stage, in which the bacteria are carried in the gut of the nematodes, and a pathogenic stage, in which susceptible insect prey are killed by the combined action of the nematode and the bacteria. Both bacteria produce antibiotics, intracellular protein crystals, and numerous other products. These traits change in phase variants, which arise when the bacteria are maintained under stationary phase conditions in the laboratory. Molecular biological studies suggest that Xenorhabdus and Photorhabdus spp. may serve as valuable model systems for studying signal transduction and transcriptional and posttranscriptional regulation of gene expression. Such studies also indicate that these bacterial groups, which had been previously considered to be very similar, may actually be quite different at the molecular level.

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Author and article information

Contributors

Chamaiporn Fukruksa: palindrome1989@hotmail.com

Thatcha Yimthin: kirari_ak@hotmail.com

Manawat Suwannaroj: starfrist@hotmail.com

Paramaporn Muangpat: m.paramaporn@gmail.com

Sarunporn Tandhavanant: sarunporn.tan@mahidol.ac.th

Aunchalee Thanwisai: aunchaleet@nu.ac.th

Apichat Vitta: apichatv@nu.ac.th

Journal

Journal ID (nlm-ta): Parasit Vectors

Journal ID (iso-abbrev): Parasit Vectors

Title: Parasites & Vectors

Publisher: BioMed Central (London )

ISSN (Electronic): 1756-3305

Publication date (Electronic): 21 September 2017

Publication date PMC-release: 21 September 2017

Publication date Collection: 2017

Volume: 10

Electronic Location Identifier: 440

Affiliations

[1 ]ISNI 0000 0000 9211 2704, GRID grid.412029.c, Department of Microbiology and Parasitology, Faculty of Medical Science, , Naresuan University, ; Phitsanulok, 65000 Thailand

[2 ]ISNI 0000 0004 1937 0490, GRID grid.10223.32, Department of Microbiology and Immunology, Faculty of Tropical Medicine, , Mahidol University, ; Bangkok, 10400 Thailand

[3 ]ISNI 0000 0000 9211 2704, GRID grid.412029.c, Centre of Excellence in Medical Biotechnology (CEMB), Faculty of Medical Science, Naresuan University, ; Phitsanulok, 65000 Thailand

[4 ]ISNI 0000 0000 9211 2704, GRID grid.412029.c, Center of Excellence for Biodiversity, Faculty of Sciences, Naresuan University, ; Phitsanulok, 65000 Thailand

Article

Publisher ID: 2383

DOI: 10.1186/s13071-017-2383-2

PMC ID: 5609025

PubMed ID: 28934970

SO-VID: 59d5c3eb-f198-45f6-806f-b7634a62429b

License:

Open AccessThis 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.

History

Date received : 23 March 2017

Date accepted : 17 September 2017

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100004944, Naresuan University;

Award ID: R2556B060

Award ID: R2559C190

Award ID: R2560B055

Award Recipient : Aunchalee Thanwisai Apichat Vitta

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ScienceOpen disciplines: Parasitology

Keywords: xenorhabdus,photorhabdus,phylogeny,larvicidal activity,aedes aegypti

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ScienceOpen disciplines: Parasitology

Keywords: xenorhabdus, photorhabdus, phylogeny, larvicidal activity, aedes aegypti

Isolation and identification of Xenorhabdus and Photorhabdus bacteria associated with entomopathogenic nematodes and their larvicidal activity against Aedes aegypti

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Abstract

Background

Results

Conclusions

Related collections

Zika Virus

Most cited references 44

Globalization, land use, and the invasion of West Nile virus.

Declining malaria, rising of dengue and Zika virus: insights for mosquito vector control.

Xenorhabdus and Photorhabdus spp.: bugs that kill bugs.

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