Nanopore metatranscriptomics reveals cryptic catfish species as potential Shigella flexneri vectors in Kenya.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
16 08 2022
16 08 2022
Historique:
received:
18
01
2022
accepted:
20
07
2022
entrez:
16
8
2022
pubmed:
17
8
2022
medline:
19
8
2022
Statut:
epublish
Résumé
Bacteria in the Shigella genus remain a major cause of dysentery in sub-Saharan Africa, and annually cause an estimated 600,000 deaths worldwide. Being spread by contaminated food and water, this study highlights how wild caught food, in the form of freshwater catfish, can act as vectors for Shigella flexneri in Southern Kenya. A metatranscriptomic approach was used to identify the presence of Shigella flexneri in the catfish which had been caught for consumption from the Galana river. The use of nanopore sequencing was shown to be a simple and effective method to highlight the presence of Shigella flexneri and could represent a potential new tool in the detection and prevention of this deadly pathogen. Rather than the presence/absence results of more traditional testing methods, the use of metatranscriptomics highlighted how primarily one SOS response gene was being transcribed, suggesting the bacteria may be dormant in the catfish. Additionally, COI sequencing of the vector catfish revealed they likely represent a cryptic species. Morphological assignment suggested the fish were widehead catfish Clarotes laticeps, which range across Africa, but the COI sequences from the Kenyan fish are distinctly different from C. laticeps sequenced in West Africa.
Identifiants
pubmed: 35974032
doi: 10.1038/s41598-022-17036-y
pii: 10.1038/s41598-022-17036-y
pmc: PMC9380665
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
13875Informations de copyright
© 2022. The Author(s).
Références
Andersen, K. G., Rambaut, A., Lipkin, W. I., Holmes, E. C. & Garry, R. F. The proximal origin of SARS-CoV-2. Nat. Med. 26, 450–452 (2020).
pubmed: 32284615
pmcid: 7095063
doi: 10.1038/s41591-020-0820-9
Warren, C. J. & Sawyer, S. L. How host genetics dictates successful viral zoonosis. PLoS Biol. 17, e3000217 (2019).
pubmed: 31002666
pmcid: 6474636
doi: 10.1371/journal.pbio.3000217
McCoy, E. et al. Foodborne agents associated with the consumption of aquaculture catfish. J. Food Prot. 74, 500–516 (2011).
pubmed: 21375890
doi: 10.4315/0362-028X.JFP-10-341
Mukwabi, D. M., Otieno, S. O., Okemo, P. O., Odour, R. O. & Agwanda, B. Parasites infesting Nile tilapia grown in aquaculture systems in Kenya. Livest. Res. Rural Dev. 31, 2–6 (2019).
Novoslavskij, A. et al. Major foodborne pathogens in fish and fish products: A review. Ann. Microbiol. 66, 1–15 (2016).
doi: 10.1007/s13213-015-1102-5
Allen, T. et al. Global hotspots and correlates of emerging zoonotic diseases. Nat. Commun. 8, 1–10 (2017).
doi: 10.1038/s41467-017-00923-8
Riede, K. Global register of migratory species: From global to regional scales: Final report of the R&D-Projekt 808 05 081. Federal Agency for Nature Conservation. (2004)
Risch, L. M. Claroteidae. In The Fresh and Brackish Water Fishes of West Africa (eds Paugy, D. et al.) 60–96 (Royal Museum for Central Africa, Tervuren, 2003).
Risch, L. M. Bagridae. In Check-List of the Freshwater Fishes of Africa (CLOFFA) (ed. Daget, J., Gosse, J. P., & Thys van den Audenaerde, D. F. E.) Vol. 2, 2–35. (ISNB, Brussels; MRAC, Tervuren; and ORSTOM, Paris, 1986)
Berg, R. W. & Anderson, A. W. Salmonellae and Edwardsiella tarda in gull feces: A source of contamination in fish processing plants. Appl. Microbiol. 24, 501–503 (1972).
pubmed: 4562484
pmcid: 376548
doi: 10.1128/am.24.3.501-503.1972
Mikaelian, I., Daignault, D., Duval, M. C. & Martineau, D. Salmonella infection in wild birds from Quebec. Can. Vet. J. 38, 385 (1997).
pubmed: 9187808
pmcid: 1576894
Koonse, B., Burkhardt, W. III., Chirtel, S. & Hoskin, G. P. Salmonella and the sanitary quality of aquacultured shrimp. J. Food Prot. 68, 2527–2532 (2005).
pubmed: 16355822
doi: 10.4315/0362-028X-68.12.2527
Jones, K. Campylobacters in water, sewage and the environment. J. Appl. Microbiol. 90, 68S-79S (2001).
doi: 10.1046/j.1365-2672.2001.01355.x
Wyatt, L. E., Nickelson, R. & Vanderzant, C. Occurrence and control of Salmonella in freshwater catfish. J. Food Sci. 44, 1067–1073 (1979).
doi: 10.1111/j.1365-2621.1979.tb03448.x
Lowry, P. W., McFarland, L. M. & Threefoot, H. K. Vibro hollisae septicemia after consumption of catfish. J. Infect. Dis. 154, 730–731 (1986).
pubmed: 3745981
doi: 10.1093/infdis/154.4.730
Tuyet, D. T. N. et al. Enteropathogenic Escherichia coli o157 in Bangui and N’Goila, Central African Republic: A brief report. Am. J. Trop. Med. Hyg. 75, 513–515 (2006).
pubmed: 16968932
doi: 10.4269/ajtmh.2006.75.513
Kotloff, K. L. et al. The incidence, aetiology, and adverse clinical consequences of less severe diarrhoeal episodes among infants and children residing in low-income and middle-income countries: a 12-month case-control study as a follow-on to the Global Enteric Multicenter Study (GEMS). Lancet Glob. Health 7, e568–e584 (2019).
pubmed: 31000128
pmcid: 6484777
doi: 10.1016/S2214-109X(19)30076-2
Shahin, K., Bouzari, M., Wang, R. & Khorasgani, M. R. Distribution of antimicrobial resistance genes and integrons among Shigella spp. isolated from water sources. J. Glob. Antimicrob. Resist. 19, 122–128 (2019).
pubmed: 31077861
doi: 10.1016/j.jgar.2019.04.020
Kinge, C. W. & Mbewe, M. Characterisation of Shigella species isolated from river catchments in the North West province of South Africa. S. Afr. J. Sci. 106, 1–4 (2010).
He, F. et al. Shigellosis outbreak associated with contaminated well water in a rural elementary school: Sichuan Province, China, June 7–16, 2009. PLoS ONE, 7, e47239 (2012).
Austin, B. Methods for the diagnosis of bacterial fish diseases. Mar. Life Sci. Technol. 1, 41–49 (2019).
doi: 10.1007/s42995-019-00002-5
Noone, J. C., Helmersen, K., Leegaard, T. M., Skråmm, I. & Aamot, H. V. Rapid diagnostics of orthopaedic-implant-associated infections using nanopore shotgun metagenomic sequencing on tissue biopsies. Microorganisms 9, 97 (2021).
pmcid: 7823515
doi: 10.3390/microorganisms9010097
Yahara, K. et al. Long-read metagenomics using PromethION uncovers oral bacteriophages and their interaction with host bacteria. Nat. Commun. 12, 1–12 (2021).
doi: 10.1038/s41467-020-20199-9
Leggett, R. M. et al. Rapid MinION profiling of preterm microbiota and antimicrobial-resistant pathogens. Nat. Microbiol. 5, 430–442 (2020).
pubmed: 31844297
doi: 10.1038/s41564-019-0626-z
Reddington, K. et al. Metagenomic analysis of planktonic riverine microbial consortia using nanopore sequencing reveals insight into river microbe taxonomy and function. GigaScience 9, 1–12 (2020).
Seegers, L., De Vos, L. & Okeyo, D. O. Annotated checklist of the freshwater fishes of Kenya (excluding the lacustrine haplochromines from Lake Victoria). J. East Afr. Nat. Hist. 92, 11–47 (2003).
doi: 10.2982/0012-8317(2003)92[11:ACOTFF]2.0.CO;2
Shabardina, V. et al. NanoPipe—a web server for nanopore MinION sequencing data analysis. GigaScience 8, giy169 (2019).
pubmed: 30689855
pmcid: 6377397
doi: 10.1093/gigascience/giy169
Ivanova, N. V., Zemlak, T. S., Hanner, R. H. & Hebert, P. D. Universal primer cocktails for fish DNA barcoding. Mol. Ecol. Notes 7, 544–548 (2007).
doi: 10.1111/j.1471-8286.2007.01748.x
Kearse, M. et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649 (2012).
pubmed: 22543367
pmcid: 3371832
doi: 10.1093/bioinformatics/bts199
Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K., von Haeseler, A. & Jermiin, L. S. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589 (2017).
pubmed: 28481363
pmcid: 5453245
doi: 10.1038/nmeth.4285
Stamatakis, A., Hoover, P. & Rougemont, J. A rapid bootstrap algorithm for the RAxML web servers. Syst. Biol. 57, 758–771 (2008).
pubmed: 18853362
doi: 10.1080/10635150802429642
Pao, G. M. & Saier, M. H. Response regulators of bacterial signal transduction systems: Selective domain shuffling during evolution. J. Mol. Evol. 40, 136–154 (1995).
pubmed: 7699720
doi: 10.1007/BF00167109
Peart, C. R., Bills, R., Wilkinson, M. & Day, J. J. Nocturnal claroteine catfishes reveal dual colonisation but a single radiation in Lake Tanganyika. Mol. Phylogenet. Evol. 73, 119–128 (2014).
pubmed: 24503480
doi: 10.1016/j.ympev.2014.01.013
Grützke, J. et al. Fishing in the soup–pathogen detection in food safety using metabarcoding and metagenomic sequencing. Front. Microbiol. 10, 1805 (2019).
pubmed: 31447815
pmcid: 6691356
doi: 10.3389/fmicb.2019.01805
Taylor, T. L. et al. Rapid, multiplexed, whole genome and plasmid sequencing of foodborne pathogens using long-read nanopore technology. Sci. Rep. 9, 1–11 (2019).
doi: 10.1038/s41598-019-52424-x
Sadek, M. et al. First genomic characterization of blaVIM-1 and mcr-9-coharbouring Enterobacter hormaechei isolated from food of animal origin. Pathogens 9, 687 (2020).
pmcid: 7558541
doi: 10.3390/pathogens9090687
Yang, M. et al. Direct metatranscriptome RNA-seq and multiplex RT-PCR amplicon sequencing on Nanopore MinION–promising strategies for multiplex identification of viable pathogens in food. Front. Microbiol. 11, 514 (2020).
pubmed: 32328039
pmcid: 7160302
doi: 10.3389/fmicb.2020.00514
Schloss, P. D. & Handelsman, J. Metagenomics for studying unculturable microorganisms: Cutting the Gordian knot. Genome Biol. 6, 1–4 (2005).
doi: 10.1186/gb-2005-6-8-229
Mani, S., Wierzba, T. & Walker, R. I. Status of vaccine research and development for Shigella. Vaccine 34, 2887–2894 (2016).
pubmed: 26979135
doi: 10.1016/j.vaccine.2016.02.075
Bowen, A. Chapter 3: Infectious diseases related to travel. In The Yellow Book: Health Information for International Travel (CDC, Florida, 2016).
Ashkenazi, S. Shigella infections in children: New insights. In Seminars in Pediatric Infectious Diseases 246–252 (WB Saunders, Philadelphia, 2004).
Miller, C., Ingmer, H., Thomsen, L. E., Skarstad, K. & Cohen, S. N. DpiA binding to the replication origin of Escherichia coli plasmids and chromosomes destabilizes plasmid inheritance and induces the bacterial SOS response. J. Bacteriol. 185, 6025–6031 (2003).
pubmed: 14526013
pmcid: 225042
doi: 10.1128/JB.185.20.6025-6031.2003
Žgur-Bertok, D. DNA damage repair and bacterial pathogens. PLoS Pathog. 9, e1003711 (2013).
pubmed: 24244154
pmcid: 3820712
doi: 10.1371/journal.ppat.1003711
Memar, M. Y. et al. The central role of the SOS DNA repair system in antibiotics resistance: A new target for a new infectious treatment strategy. Life Sci. 262, 118562 (2020).
pubmed: 33038378
doi: 10.1016/j.lfs.2020.118562
Shi, R. et al. Pathogenicity of Shigella in chickens. PLoS ONE 9, e100264 (2014).
pubmed: 24949637
pmcid: 4064985
doi: 10.1371/journal.pone.0100264
Jianjun, J. Isolation and identification of rabbits Shigella dysenteriae in a large scale warren. J. Anhui Agric. Sci. 33, 1666 (2005).
Zhu, Z., Cao, M., Zhou, X., Li, B. & Zhang, J. Epidemic characterization and molecular genotyping of Shigella flexneri isolated from calves with diarrhea in Northwest China. Antimicrob. Resist. Infect. Control 6, 1–11 (2017).
doi: 10.1186/s13756-017-0252-6
Maurelli, A. T. et al. Shigellainfection as observed in the experimentally inoculated domestic pig, Sus scrofa domestica. Microbial. Pathog. 25, 189–196 (1998).
doi: 10.1006/mpat.1998.0230
Dudley, J. P. et al. Carnivory in the common hippopotamus Hippopotamus amphibius: Implications for the ecology and epidemiology of anthrax in African landscapes. Mamm. Rev. 46, 191–203 (2016).
doi: 10.1111/mam.12056
Murphree, R., Warkentin, J. V., Dunn, J. R., Schaffner, W. & Jones, T. F. Elephant-to-human transmission of tuberculosis, 2009. Emerg. Infect. Dis. 17, 366 (2011).
pubmed: 21392425
pmcid: 3166032
doi: 10.3201/eid1703.101668
Kapetsky, J. M., & Petr, T. Status of African reservoir fisheries. FAO (1984).
Eccles, D. H. FAO species identification sheets for fishery purposes. In Field Guide to the Freshwater Fishes of Tanzania (FAO, Rome, 1992).
Nwani, C. D. et al. DNA barcoding discriminates freshwater fishes from southeastern Nigeria and provides river system-level phylogeographic resolution within some species. Mitochondrial DNA 22, 43–51 (2011).
pubmed: 21406042
doi: 10.3109/19401736.2010.536537
Okeyo, D. O. Updating names, distribution and ecology of riverine fish of Kenya in the Athi-Galana-Sabaki River drainage system, Naga. ICLARM Q. 21, 44–53 (1998).