The Tripartite Associations between Bacteriophage, Wolbachia, and Arthropods

By manipulating arthropod reproduction worldwide, the heritable endosymbiont Wolbachia has spread to pandemic levels. Little is known about the microbial basis of cytoplasmic incompatibility (CI) except that bacterial densities and percentages of infected sperm cysts associate with incompatibility s...

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Autores principales: Bordenstein, Seth R, Marshall, Michelle L, Fry, Adam J, Kim, Ulandt, Wernegreen, Jennifer J
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2006
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1463016/
https://www.ncbi.nlm.nih.gov/pubmed/16710453
http://dx.doi.org/10.1371/journal.ppat.0020043
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author Bordenstein, Seth R
Marshall, Michelle L
Fry, Adam J
Kim, Ulandt
Wernegreen, Jennifer J
author_facet Bordenstein, Seth R
Marshall, Michelle L
Fry, Adam J
Kim, Ulandt
Wernegreen, Jennifer J
author_sort Bordenstein, Seth R
collection PubMed
description By manipulating arthropod reproduction worldwide, the heritable endosymbiont Wolbachia has spread to pandemic levels. Little is known about the microbial basis of cytoplasmic incompatibility (CI) except that bacterial densities and percentages of infected sperm cysts associate with incompatibility strength. The recent discovery of a temperate bacteriophage (WO-B) of Wolbachia containing ankyrin-encoding genes and virulence factors has led to intensifying debate that bacteriophage WO-B induces CI. However, current hypotheses have not considered the separate roles that lytic and lysogenic phage might have on bacterial fitness and phenotype. Here we describe a set of quantitative approaches to characterize phage densities and its associations with bacterial densities and CI. We enumerated genome copy number of phage WO-B and Wolbachia and CI penetrance in supergroup A- and B-infected males of the parasitoid wasp Nasonia vitripennis. We report several findings: (1) variability in CI strength for A-infected males is positively associated with bacterial densities, as expected under the bacterial density model of CI, (2) phage and bacterial densities have a significant inverse association, as expected for an active lytic infection, and (3) CI strength and phage densities are inversely related in A-infected males; similarly, males expressing incomplete CI have significantly higher phage densities than males expressing complete CI. Ultrastructural analyses indicate that approximately 12% of the A Wolbachia have phage particles, and aggregations of these particles can putatively occur outside the Wolbachia cell. Physical interactions were observed between approximately 16% of the Wolbachia cells and spermatid tails. The results support a low to moderate frequency of lytic development in Wolbachia and an overall negative density relationship between bacteriophage and Wolbachia. The findings motivate a novel phage density model of CI in which lytic phage repress Wolbachia densities and therefore reproductive parasitism. We conclude that phage, Wolbachia, and arthropods form a tripartite symbiotic association in which all three are integral to understanding the biology of this widespread endosymbiosis. Clarifying the roles of lytic and lysogenic phage development in Wolbachia biology will effectively structure inquiries into this research topic.
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spelling pubmed-14630162006-05-26 The Tripartite Associations between Bacteriophage, Wolbachia, and Arthropods Bordenstein, Seth R Marshall, Michelle L Fry, Adam J Kim, Ulandt Wernegreen, Jennifer J PLoS Pathog Research Article By manipulating arthropod reproduction worldwide, the heritable endosymbiont Wolbachia has spread to pandemic levels. Little is known about the microbial basis of cytoplasmic incompatibility (CI) except that bacterial densities and percentages of infected sperm cysts associate with incompatibility strength. The recent discovery of a temperate bacteriophage (WO-B) of Wolbachia containing ankyrin-encoding genes and virulence factors has led to intensifying debate that bacteriophage WO-B induces CI. However, current hypotheses have not considered the separate roles that lytic and lysogenic phage might have on bacterial fitness and phenotype. Here we describe a set of quantitative approaches to characterize phage densities and its associations with bacterial densities and CI. We enumerated genome copy number of phage WO-B and Wolbachia and CI penetrance in supergroup A- and B-infected males of the parasitoid wasp Nasonia vitripennis. We report several findings: (1) variability in CI strength for A-infected males is positively associated with bacterial densities, as expected under the bacterial density model of CI, (2) phage and bacterial densities have a significant inverse association, as expected for an active lytic infection, and (3) CI strength and phage densities are inversely related in A-infected males; similarly, males expressing incomplete CI have significantly higher phage densities than males expressing complete CI. Ultrastructural analyses indicate that approximately 12% of the A Wolbachia have phage particles, and aggregations of these particles can putatively occur outside the Wolbachia cell. Physical interactions were observed between approximately 16% of the Wolbachia cells and spermatid tails. The results support a low to moderate frequency of lytic development in Wolbachia and an overall negative density relationship between bacteriophage and Wolbachia. The findings motivate a novel phage density model of CI in which lytic phage repress Wolbachia densities and therefore reproductive parasitism. We conclude that phage, Wolbachia, and arthropods form a tripartite symbiotic association in which all three are integral to understanding the biology of this widespread endosymbiosis. Clarifying the roles of lytic and lysogenic phage development in Wolbachia biology will effectively structure inquiries into this research topic. Public Library of Science 2006-05 2006-05-19 /pmc/articles/PMC1463016/ /pubmed/16710453 http://dx.doi.org/10.1371/journal.ppat.0020043 Text en © 2006 Bordenstein et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Bordenstein, Seth R
Marshall, Michelle L
Fry, Adam J
Kim, Ulandt
Wernegreen, Jennifer J
The Tripartite Associations between Bacteriophage, Wolbachia, and Arthropods
title The Tripartite Associations between Bacteriophage, Wolbachia, and Arthropods
title_full The Tripartite Associations between Bacteriophage, Wolbachia, and Arthropods
title_fullStr The Tripartite Associations between Bacteriophage, Wolbachia, and Arthropods
title_full_unstemmed The Tripartite Associations between Bacteriophage, Wolbachia, and Arthropods
title_short The Tripartite Associations between Bacteriophage, Wolbachia, and Arthropods
title_sort tripartite associations between bacteriophage, wolbachia, and arthropods
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1463016/
https://www.ncbi.nlm.nih.gov/pubmed/16710453
http://dx.doi.org/10.1371/journal.ppat.0020043
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