Symbiotic bacteria associated with entomopathogenic nematodes showed molluscicidal activity against Biomphalaria glabrata, an intermediate host of Schistosoma mansoni
Abstract Background Biomphalaria glabrata acts as the intermediate host of schistosomes that causes human schistosomiasis. Symbiotic bacteria, Xenorhabdus and Photorhabdus associated with Steinernema and Heterorhabditis, produce secondary metabolites with several biological activities. Controlling B...
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2024-12-01
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| Series: | Parasites & Vectors |
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| Online Access: | https://doi.org/10.1186/s13071-024-06605-x |
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| author | Jiranun Ardpairin Chanakan Subkrasae Abdulhakam Dumidae Supawan Pansri Chanatinat Homkaew Wipanee Meesil Tewarat Kumchantuek Ittipon Phoungpetchara Adler R. Dillman Coralie Pavesi Helge B. Bode Sarunporn Tandhavanant Aunchalee Thanwisai Apichat Vitta |
| author_facet | Jiranun Ardpairin Chanakan Subkrasae Abdulhakam Dumidae Supawan Pansri Chanatinat Homkaew Wipanee Meesil Tewarat Kumchantuek Ittipon Phoungpetchara Adler R. Dillman Coralie Pavesi Helge B. Bode Sarunporn Tandhavanant Aunchalee Thanwisai Apichat Vitta |
| author_sort | Jiranun Ardpairin |
| collection | DOAJ |
| description | Abstract Background Biomphalaria glabrata acts as the intermediate host of schistosomes that causes human schistosomiasis. Symbiotic bacteria, Xenorhabdus and Photorhabdus associated with Steinernema and Heterorhabditis, produce secondary metabolites with several biological activities. Controlling B. glabrata is a potential strategy to limit the transmission of schistosomiasis. The aims of this study were to identify Xenorhabdus and Photorhabdus bacteria based on recA sequencing and evaluate their molluscicidal activity against B. glabrata snail. Results A total of 31 bacterial isolates belonging to Xenorhabdus (n = 19) and Photorhabdus (n = 12) (X. ehlersii, X. stockiae, X. indica, X. griffinae, P. luminescens, P. akhurstii, and P. laumondii subsp. laumondii were molecularly identified based on recA sequencing. Five isolates of bacterial extracts showed potential molluscicide, with 100% snail mortality. P. laumondii subsp. laumondii (bALN19.5_TH) showed the highest effectiveness with lethal concentration (LC) values of 54.52 µg/mL and 89.58 µg/mL for LC50 and LC90, respectively. Histopathological changes of the snail were observed in the head–foot region, which showed ruptures of the epithelium covering the foot and deformation of the muscle fiber. A hemocyte of the treated snails was observed in the digestive tubules of the digestive glands. The hermaphrodite glands of treated snails showed a reduction in the number of spermatozoa, degeneration of oocytes, and deformation and destruction in the hermaphrodite gland. In addition, liquid chromatography–tandem mass spectrometry (LC–MS/MS) of three symbiotic bacteria contained compounds such as GameXPeptide, Xenofuranone, and Rhabdopeptide. Conclusions Five bacterial extracts showed good activity against B. glabrata, especially P. laumondii subsp. laumondii and X. stockiae, which produced virulent secondary metabolites resulting in the death of the snails. They also caused histopathological alterations in the foot, digestive glands, and hermaphrodite glands of the snails. This study suggests that extracts from these bacteria show promise as molluscicides for the control of B. glabrata. Graphical abstract |
| format | Article |
| id | doaj-art-e64fe8b6fbbd4af586bf3de6addfac80 |
| institution | DOAJ |
| issn | 1756-3305 |
| language | English |
| publishDate | 2024-12-01 |
| publisher | BMC |
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| series | Parasites & Vectors |
| spelling | doaj-art-e64fe8b6fbbd4af586bf3de6addfac802025-08-20T02:57:32ZengBMCParasites & Vectors1756-33052024-12-0117111610.1186/s13071-024-06605-xSymbiotic bacteria associated with entomopathogenic nematodes showed molluscicidal activity against Biomphalaria glabrata, an intermediate host of Schistosoma mansoniJiranun Ardpairin0Chanakan Subkrasae1Abdulhakam Dumidae2Supawan Pansri3Chanatinat Homkaew4Wipanee Meesil5Tewarat Kumchantuek6Ittipon Phoungpetchara7Adler R. Dillman8Coralie Pavesi9Helge B. Bode10Sarunporn Tandhavanant11Aunchalee Thanwisai12Apichat Vitta13Department of Microbiology and Parasitology, Faculty of Medical Science, Naresuan UniversityDepartment of Microbiology and Parasitology, Faculty of Medical Science, Naresuan UniversityDepartment of Microbiology and Parasitology, Faculty of Medical Science, Naresuan UniversityDepartment of Microbiology and Parasitology, Faculty of Medical Science, Naresuan UniversityDepartment of Microbiology and Parasitology, Faculty of Medical Science, Naresuan UniversityDepartment of Microbiology and Parasitology, Faculty of Medical Science, Naresuan UniversityDepartment of Anatomy, Faculty of Medical Science, Naresuan UniversityDepartment of Anatomy, Faculty of Medical Science, Naresuan UniversityDepartment of Nematology, University of CaliforniaMax-Planck-Institut für Terrestrische Mikrobiologie Abteilung Naturstoffe in organismischen InteraktionenMax-Planck-Institut für Terrestrische Mikrobiologie Abteilung Naturstoffe in organismischen InteraktionenDepartment of Microbiology and Immunology, Faculty of Tropical Medicine, Mahidol UniversityDepartment of Microbiology and Parasitology, Faculty of Medical Science, Naresuan UniversityDepartment of Microbiology and Parasitology, Faculty of Medical Science, Naresuan UniversityAbstract Background Biomphalaria glabrata acts as the intermediate host of schistosomes that causes human schistosomiasis. Symbiotic bacteria, Xenorhabdus and Photorhabdus associated with Steinernema and Heterorhabditis, produce secondary metabolites with several biological activities. Controlling B. glabrata is a potential strategy to limit the transmission of schistosomiasis. The aims of this study were to identify Xenorhabdus and Photorhabdus bacteria based on recA sequencing and evaluate their molluscicidal activity against B. glabrata snail. Results A total of 31 bacterial isolates belonging to Xenorhabdus (n = 19) and Photorhabdus (n = 12) (X. ehlersii, X. stockiae, X. indica, X. griffinae, P. luminescens, P. akhurstii, and P. laumondii subsp. laumondii were molecularly identified based on recA sequencing. Five isolates of bacterial extracts showed potential molluscicide, with 100% snail mortality. P. laumondii subsp. laumondii (bALN19.5_TH) showed the highest effectiveness with lethal concentration (LC) values of 54.52 µg/mL and 89.58 µg/mL for LC50 and LC90, respectively. Histopathological changes of the snail were observed in the head–foot region, which showed ruptures of the epithelium covering the foot and deformation of the muscle fiber. A hemocyte of the treated snails was observed in the digestive tubules of the digestive glands. The hermaphrodite glands of treated snails showed a reduction in the number of spermatozoa, degeneration of oocytes, and deformation and destruction in the hermaphrodite gland. In addition, liquid chromatography–tandem mass spectrometry (LC–MS/MS) of three symbiotic bacteria contained compounds such as GameXPeptide, Xenofuranone, and Rhabdopeptide. Conclusions Five bacterial extracts showed good activity against B. glabrata, especially P. laumondii subsp. laumondii and X. stockiae, which produced virulent secondary metabolites resulting in the death of the snails. They also caused histopathological alterations in the foot, digestive glands, and hermaphrodite glands of the snails. This study suggests that extracts from these bacteria show promise as molluscicides for the control of B. glabrata. Graphical abstracthttps://doi.org/10.1186/s13071-024-06605-xEntomopathogenic nematodeHistological alterationSchistosomeSnailSymbiotic bacteria |
| spellingShingle | Jiranun Ardpairin Chanakan Subkrasae Abdulhakam Dumidae Supawan Pansri Chanatinat Homkaew Wipanee Meesil Tewarat Kumchantuek Ittipon Phoungpetchara Adler R. Dillman Coralie Pavesi Helge B. Bode Sarunporn Tandhavanant Aunchalee Thanwisai Apichat Vitta Symbiotic bacteria associated with entomopathogenic nematodes showed molluscicidal activity against Biomphalaria glabrata, an intermediate host of Schistosoma mansoni Parasites & Vectors Entomopathogenic nematode Histological alteration Schistosome Snail Symbiotic bacteria |
| title | Symbiotic bacteria associated with entomopathogenic nematodes showed molluscicidal activity against Biomphalaria glabrata, an intermediate host of Schistosoma mansoni |
| title_full | Symbiotic bacteria associated with entomopathogenic nematodes showed molluscicidal activity against Biomphalaria glabrata, an intermediate host of Schistosoma mansoni |
| title_fullStr | Symbiotic bacteria associated with entomopathogenic nematodes showed molluscicidal activity against Biomphalaria glabrata, an intermediate host of Schistosoma mansoni |
| title_full_unstemmed | Symbiotic bacteria associated with entomopathogenic nematodes showed molluscicidal activity against Biomphalaria glabrata, an intermediate host of Schistosoma mansoni |
| title_short | Symbiotic bacteria associated with entomopathogenic nematodes showed molluscicidal activity against Biomphalaria glabrata, an intermediate host of Schistosoma mansoni |
| title_sort | symbiotic bacteria associated with entomopathogenic nematodes showed molluscicidal activity against biomphalaria glabrata an intermediate host of schistosoma mansoni |
| topic | Entomopathogenic nematode Histological alteration Schistosome Snail Symbiotic bacteria |
| url | https://doi.org/10.1186/s13071-024-06605-x |
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