{"title":"Guild Dynamics and Pathogen Interactions in Hyalomma Ticks From Algerian Cattle","authors":"Salma Kaoutar Abdelali, Lynda Aissaoui, Apolline Maitre, Elianne Piloto-Sardiñas, Constance Julie, Angélique Foucault-Simonin, Sara Moutailler, Clemence Galon, Lourdes Mateos-Hernández, Dasiel Obregon, Zbigniew Zając, Alejandro Cabezas-Cruz","doi":"10.1155/tbed/5384559","DOIUrl":null,"url":null,"abstract":"<div>\n <p>Ticks are pivotal in transmitting a variety of pathogens that affect both humans and animals. These pathogens often occur in guilds, groups of species that exploit similar resources in similar ways. Although the composition of tick-borne pathogen (TBP) guilds is well-documented, the interactions among pathogens within these guilds remain poorly understood. We hypothesized that abiotic and biotic factors significantly influence the patterns of occurrence and interactions among pathogens within these guilds. To investigate this, we analyzed microfluidic-based high-throughput data on microorganisms from 166 <i>Hyalomma excavatum</i> ticks (94 male and 72 female) collected across different seasons from cattle in the central Algerian steppe using network analysis to uncover complex pathogen–pathogen interaction patterns. We found that female ticks had a higher infection rate (63.9%) with common pathogens such as <i>Rickettsia slovaca</i> (26.4%), unclassified Apicomplexa (22.2%), and <i>Borrelia afzelii</i> (19.4%). Male ticks showed a 56.4% infection rate, with <i>Rickettsia</i> (31.1%) and <i>R. slovaca</i> (16%) being the most prevalent. Notable pathogen–pathogen interactions within guilds were identified, with positive associations such as between <i>R. slovaca</i> and <i>Rickettsia conorii</i> in males, and <i>B. afzelii</i> and <i>Borrelia spielmanii</i> in females, indicating cooperative interactions. Conversely, negative associations, such as between <i>Anaplasma phagocytophilum</i> and <i>Francisella tularensis</i>, suggested competitive exclusion. The observed variation in interaction patterns under different conditions indicates that ecological determinants, both biotic and abiotic, influence pathogen association dynamics within guilds. These findings have significant implications for understanding disease transmission and developing control strategies.</p>\n </div>","PeriodicalId":234,"journal":{"name":"Transboundary and Emerging Diseases","volume":"2024 1","pages":""},"PeriodicalIF":3.5000,"publicationDate":"2024-12-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1155/tbed/5384559","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Transboundary and Emerging Diseases","FirstCategoryId":"97","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1155/tbed/5384559","RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"INFECTIOUS DISEASES","Score":null,"Total":0}
引用次数: 0
Abstract
Ticks are pivotal in transmitting a variety of pathogens that affect both humans and animals. These pathogens often occur in guilds, groups of species that exploit similar resources in similar ways. Although the composition of tick-borne pathogen (TBP) guilds is well-documented, the interactions among pathogens within these guilds remain poorly understood. We hypothesized that abiotic and biotic factors significantly influence the patterns of occurrence and interactions among pathogens within these guilds. To investigate this, we analyzed microfluidic-based high-throughput data on microorganisms from 166 Hyalomma excavatum ticks (94 male and 72 female) collected across different seasons from cattle in the central Algerian steppe using network analysis to uncover complex pathogen–pathogen interaction patterns. We found that female ticks had a higher infection rate (63.9%) with common pathogens such as Rickettsia slovaca (26.4%), unclassified Apicomplexa (22.2%), and Borrelia afzelii (19.4%). Male ticks showed a 56.4% infection rate, with Rickettsia (31.1%) and R. slovaca (16%) being the most prevalent. Notable pathogen–pathogen interactions within guilds were identified, with positive associations such as between R. slovaca and Rickettsia conorii in males, and B. afzelii and Borrelia spielmanii in females, indicating cooperative interactions. Conversely, negative associations, such as between Anaplasma phagocytophilum and Francisella tularensis, suggested competitive exclusion. The observed variation in interaction patterns under different conditions indicates that ecological determinants, both biotic and abiotic, influence pathogen association dynamics within guilds. These findings have significant implications for understanding disease transmission and developing control strategies.
期刊介绍:
Transboundary and Emerging Diseases brings together in one place the latest research on infectious diseases considered to hold the greatest economic threat to animals and humans worldwide. The journal provides a venue for global research on their diagnosis, prevention and management, and for papers on public health, pathogenesis, epidemiology, statistical modeling, diagnostics, biosecurity issues, genomics, vaccine development and rapid communication of new outbreaks. Papers should include timely research approaches using state-of-the-art technologies. The editors encourage papers adopting a science-based approach on socio-economic and environmental factors influencing the management of the bio-security threat posed by these diseases, including risk analysis and disease spread modeling. Preference will be given to communications focusing on novel science-based approaches to controlling transboundary and emerging diseases. The following topics are generally considered out-of-scope, but decisions are made on a case-by-case basis (for example, studies on cryptic wildlife populations, and those on potential species extinctions):
Pathogen discovery: a common pathogen newly recognised in a specific country, or a new pathogen or genetic sequence for which there is little context about — or insights regarding — its emergence or spread.
Prevalence estimation surveys and risk factor studies based on survey (rather than longitudinal) methodology, except when such studies are unique. Surveys of knowledge, attitudes and practices are within scope.
Diagnostic test development if not accompanied by robust sensitivity and specificity estimation from field studies.
Studies focused only on laboratory methods in which relevance to disease emergence and spread is not obvious or can not be inferred (“pure research” type studies).
Narrative literature reviews which do not generate new knowledge. Systematic and scoping reviews, and meta-analyses are within scope.