Differential nested patterns of Anaplasma marginale and Coxiella-like endosymbiont across Rhipicephalus microplus ontogeny

Understanding the intricate ecological interactions within the microbiome of arthropod vectors is crucial for elucidating disease transmission dynamics and developing effective control strategies. In this study, we investigated the ecological roles of Coxiella-like endosymbiont (CLE) and Anaplasma m...

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Published in:Microbiological research Vol. 286; p. 127790
Main Authors: Abuin-Denis, Lianet, Piloto-Sardiñas, Elianne, Maitre, Apolline, Wu-Chuang, Alejandra, Mateos-Hernández, Lourdes, Paulino, Patrícia Gonzaga, Bello, Yamil, Bravo, Frank Ledesma, Gutierrez, Anays Alvarez, Fernández, Rafmary Rodríguez, Castillo, Alier Fuentes, Mellor, Luis Méndez, Foucault-Simonin, Angélique, Obregon, Dasiel, Estrada-García, Mario Pablo, Rodríguez-Mallon, Alina, Cabezas-Cruz, Alejandro
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Abstract Understanding the intricate ecological interactions within the microbiome of arthropod vectors is crucial for elucidating disease transmission dynamics and developing effective control strategies. In this study, we investigated the ecological roles of Coxiella-like endosymbiont (CLE) and Anaplasma marginale across larval, nymphal, and adult stages of Rhipicephalus microplus. We hypothesized that CLE would show a stable, nested pattern reflecting co-evolution with the tick host, while A. marginale would exhibit a more dynamic, non-nested pattern influenced by environmental factors and host immune responses. Our findings revealed a stable, nested pattern characteristic of co-evolutionary mutualism for CLE, occurring in all developmental stages of the tick. Conversely, A. marginale exhibited variable occurrence but exerted significant influence on microbial community structure, challenging our initial hypotheses of its non-nested dynamics. Furthermore, in silico removal of both microbes from the co-occurrence networks altered network topology, underscoring their central roles in the R. microplus microbiome. Notably, competitive interactions between CLE and A. marginale were observed in nymphal network, potentially reflecting the impact of CLE on the pathogen transstadial-transmission. These findings shed light on the complex ecological dynamics within tick microbiomes and have implications for disease management strategies.
AbstractList Understanding the intricate ecological interactions within the microbiome of arthropod vectors is crucial for elucidating disease transmission dynamics and developing effective control strategies. In this study, we investigated the ecological roles of Coxiella-like endosymbiont (CLE) and Anaplasma marginale across larval, nymphal, and adult stages of Rhipicephalus microplus. We hypothesized that CLE would show a stable, nested pattern reflecting co-evolution with the tick host, while A. marginale would exhibit a more dynamic, non-nested pattern influenced by environmental factors and host immune responses. Our findings revealed a stable, nested pattern characteristic of co-evolutionary mutualism for CLE, occurring in all developmental stages of the tick. Conversely, A. marginale exhibited variable occurrence but exerted significant influence on microbial community structure, challenging our initial hypotheses of its non-nested dynamics. Furthermore, in silico removal of both microbes from the co-occurrence networks altered network topology, underscoring their central roles in the R. microplus microbiome. Notably, competitive interactions between CLE and A. marginale were observed in nymphal network, potentially reflecting the impact of CLE on the pathogen transstadial-transmission. These findings shed light on the complex ecological dynamics within tick microbiomes and have implications for disease management strategies.
Understanding the intricate ecological interactions within the microbiome of arthropod vectors is crucial for elucidating disease transmission dynamics and developing effective control strategies. In this study, we investigated the ecological roles of Coxiella-like endosymbiont (CLE) and Anaplasma marginale across larval, nymphal, and adult stages of Rhipicephalus microplus. We hypothesized that CLE would show a stable, nested pattern reflecting co-evolution with the tick host, while A. marginale would exhibit a more dynamic, non-nested pattern influenced by environmental factors and host immune responses. Our findings revealed a stable, nested pattern characteristic of co-evolutionary mutualism for CLE, occurring in all developmental stages of the tick. Conversely, A. marginale exhibited variable occurrence but exerted significant influence on microbial community structure, challenging our initial hypotheses of its non-nested dynamics. Furthermore, in silico removal of both microbes from the co-occurrence networks altered network topology, underscoring their central roles in the R. microplus microbiome. Notably, competitive interactions between CLE and A. marginale were observed in nymphal network, potentially reflecting the impact of CLE on the pathogen transstadial-transmission. These findings shed light on the complex ecological dynamics within tick microbiomes and have implications for disease management strategies.Understanding the intricate ecological interactions within the microbiome of arthropod vectors is crucial for elucidating disease transmission dynamics and developing effective control strategies. In this study, we investigated the ecological roles of Coxiella-like endosymbiont (CLE) and Anaplasma marginale across larval, nymphal, and adult stages of Rhipicephalus microplus. We hypothesized that CLE would show a stable, nested pattern reflecting co-evolution with the tick host, while A. marginale would exhibit a more dynamic, non-nested pattern influenced by environmental factors and host immune responses. Our findings revealed a stable, nested pattern characteristic of co-evolutionary mutualism for CLE, occurring in all developmental stages of the tick. Conversely, A. marginale exhibited variable occurrence but exerted significant influence on microbial community structure, challenging our initial hypotheses of its non-nested dynamics. Furthermore, in silico removal of both microbes from the co-occurrence networks altered network topology, underscoring their central roles in the R. microplus microbiome. Notably, competitive interactions between CLE and A. marginale were observed in nymphal network, potentially reflecting the impact of CLE on the pathogen transstadial-transmission. These findings shed light on the complex ecological dynamics within tick microbiomes and have implications for disease management strategies.
ArticleNumber 127790
Author Estrada-García, Mario Pablo
Bravo, Frank Ledesma
Wu-Chuang, Alejandra
Mellor, Luis Méndez
Mateos-Hernández, Lourdes
Cabezas-Cruz, Alejandro
Gutierrez, Anays Alvarez
Paulino, Patrícia Gonzaga
Abuin-Denis, Lianet
Bello, Yamil
Castillo, Alier Fuentes
Rodríguez-Mallon, Alina
Obregon, Dasiel
Piloto-Sardiñas, Elianne
Maitre, Apolline
Fernández, Rafmary Rodríguez
Foucault-Simonin, Angélique
Author_xml – sequence: 1
  givenname: Lianet
  surname: Abuin-Denis
  fullname: Abuin-Denis, Lianet
  organization: Animal Biotechnology Department, Center for Genetic Engineering and Biotechnology, Avenue 31 between 158 and 190, P.O. Box 6162, Havana 10600, Cuba
– sequence: 2
  givenname: Elianne
  surname: Piloto-Sardiñas
  fullname: Piloto-Sardiñas, Elianne
  organization: ANSES, INRAE, Ecole Nationale Vétérinaire d’Alfort, UMR BIPAR, Laboratoire de Santé Animale, Maisons-Alfort F-94700, France
– sequence: 3
  givenname: Apolline
  surname: Maitre
  fullname: Maitre, Apolline
  organization: ANSES, INRAE, Ecole Nationale Vétérinaire d’Alfort, UMR BIPAR, Laboratoire de Santé Animale, Maisons-Alfort F-94700, France
– sequence: 4
  givenname: Alejandra
  surname: Wu-Chuang
  fullname: Wu-Chuang, Alejandra
  organization: ANSES, INRAE, Ecole Nationale Vétérinaire d’Alfort, UMR BIPAR, Laboratoire de Santé Animale, Maisons-Alfort F-94700, France
– sequence: 5
  givenname: Lourdes
  surname: Mateos-Hernández
  fullname: Mateos-Hernández, Lourdes
  organization: ANSES, INRAE, Ecole Nationale Vétérinaire d’Alfort, UMR BIPAR, Laboratoire de Santé Animale, Maisons-Alfort F-94700, France
– sequence: 6
  givenname: Patrícia Gonzaga
  surname: Paulino
  fullname: Paulino, Patrícia Gonzaga
  organization: Department of Epidemiology and Public Health, Federal Rural University of Rio de Janeiro (UFRRJ), Seropedica 23890-000, Brazil
– sequence: 7
  givenname: Yamil
  surname: Bello
  fullname: Bello, Yamil
  organization: Animal Biotechnology Department, Center for Genetic Engineering and Biotechnology, Avenue 31 between 158 and 190, P.O. Box 6162, Havana 10600, Cuba
– sequence: 8
  givenname: Frank Ledesma
  surname: Bravo
  fullname: Bravo, Frank Ledesma
  organization: Animal Biotechnology Department, Center for Genetic Engineering and Biotechnology, Avenue 31 between 158 and 190, P.O. Box 6162, Havana 10600, Cuba
– sequence: 9
  givenname: Anays Alvarez
  surname: Gutierrez
  fullname: Gutierrez, Anays Alvarez
  organization: Animal Biotechnology Department, Center for Genetic Engineering and Biotechnology, Avenue 31 between 158 and 190, P.O. Box 6162, Havana 10600, Cuba
– sequence: 10
  givenname: Rafmary Rodríguez
  surname: Fernández
  fullname: Fernández, Rafmary Rodríguez
  organization: National Laboratory of Parasitology, Ministry of Agriculture, Autopista San Antonio de los Baños, Km 112, San Antonio de los Baños, Artemisa 38100, Cuba
– sequence: 11
  givenname: Alier Fuentes
  surname: Castillo
  fullname: Castillo, Alier Fuentes
  organization: National Laboratory of Parasitology, Ministry of Agriculture, Autopista San Antonio de los Baños, Km 112, San Antonio de los Baños, Artemisa 38100, Cuba
– sequence: 12
  givenname: Luis Méndez
  surname: Mellor
  fullname: Mellor, Luis Méndez
  organization: National Laboratory of Parasitology, Ministry of Agriculture, Autopista San Antonio de los Baños, Km 112, San Antonio de los Baños, Artemisa 38100, Cuba
– sequence: 13
  givenname: Angélique
  surname: Foucault-Simonin
  fullname: Foucault-Simonin, Angélique
  organization: ANSES, INRAE, Ecole Nationale Vétérinaire d’Alfort, UMR BIPAR, Laboratoire de Santé Animale, Maisons-Alfort F-94700, France
– sequence: 14
  givenname: Dasiel
  surname: Obregon
  fullname: Obregon, Dasiel
  organization: School of Environmental Sciences University of Guelph, Guelph, Ontario N1G 2W1, Canada
– sequence: 15
  givenname: Mario Pablo
  surname: Estrada-García
  fullname: Estrada-García, Mario Pablo
  organization: Animal Biotechnology Department, Center for Genetic Engineering and Biotechnology, Avenue 31 between 158 and 190, P.O. Box 6162, Havana 10600, Cuba
– sequence: 16
  givenname: Alina
  surname: Rodríguez-Mallon
  fullname: Rodríguez-Mallon, Alina
  email: alina.rodriguez@cigb.edu.cu
  organization: Animal Biotechnology Department, Center for Genetic Engineering and Biotechnology, Avenue 31 between 158 and 190, P.O. Box 6162, Havana 10600, Cuba
– sequence: 17
  givenname: Alejandro
  surname: Cabezas-Cruz
  fullname: Cabezas-Cruz, Alejandro
  email: alejandro.cabezas@vet-alfort.fr
  organization: ANSES, INRAE, Ecole Nationale Vétérinaire d’Alfort, UMR BIPAR, Laboratoire de Santé Animale, Maisons-Alfort F-94700, France
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Keywords Tick-borne pathogens
Ticks
Community assembly
Tick -borne disease
Tick
Language English
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Snippet Understanding the intricate ecological interactions within the microbiome of arthropod vectors is crucial for elucidating disease transmission dynamics and...
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SubjectTerms Anaplasma marginale
Animals
Community assembly
Coxiella - genetics
Ecology, environment
Larva - growth & development
Larva - microbiology
Life Sciences
Microbiota
Nymph - growth & development
Nymph - microbiology
Rhipicephalus - microbiology
Symbiosis
Tick-borne pathogens
Ticks
Title Differential nested patterns of Anaplasma marginale and Coxiella-like endosymbiont across Rhipicephalus microplus ontogeny
URI https://dx.doi.org/10.1016/j.micres.2024.127790
https://www.ncbi.nlm.nih.gov/pubmed/38851009
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https://hal.science/hal-04633489
Volume 286
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