Mutualism breakdown by amplification of Wolbachia genes.
Most insect species are associated with vertically transmitted endosymbionts. Because of the mode of transmission, the fitness of these symbionts is dependent on the fitness of the hosts. Therefore, these endosymbionts need to control their proliferation in order to minimize their cost for the host....
| Main Authors: | , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2015-02-01
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| Series: | PLoS Biology |
| Online Access: | https://doi.org/10.1371/journal.pbio.1002065 |
| _version_ | 1818918820631281664 |
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| author | Ewa Chrostek Luis Teixeira |
| author_facet | Ewa Chrostek Luis Teixeira |
| author_sort | Ewa Chrostek |
| collection | DOAJ |
| description | Most insect species are associated with vertically transmitted endosymbionts. Because of the mode of transmission, the fitness of these symbionts is dependent on the fitness of the hosts. Therefore, these endosymbionts need to control their proliferation in order to minimize their cost for the host. The genetic bases and mechanisms of this regulation remain largely undetermined. The maternally inherited bacteria of the genus Wolbachia are the most common endosymbionts of insects, providing some of them with fitness benefits. In Drosophila melanogaster, Wolbachia wMelPop is a unique virulent variant that proliferates massively in the hosts and shortens their lifespan. The genetic bases of wMelPop virulence are unknown, and their identification would allow a better understanding of how Wolbachia levels are regulated. Here we show that amplification of a region containing eight Wolbachia genes, called Octomom, is responsible for wMelPop virulence. Using Drosophila lines selected for carrying Wolbachia with different Octomom copy numbers, we demonstrate that the number of Octomom copies determines Wolbachia titers and the strength of the lethal phenotype. Octomom amplification is unstable, and reversion of copy number to one reverts all the phenotypes. Our results provide a link between genotype and phenotype in Wolbachia and identify a genomic region regulating Wolbachia proliferation. We also prove that these bacteria can evolve rapidly. Rapid evolution by changes in gene copy number may be common in endosymbionts with a high number of mobile elements and other repeated regions. Understanding wMelPop pathogenicity and variability also allows researchers to better control and predict the outcome of releasing mosquitoes transinfected with this variant to block human vector-borne diseases. Our results show that transition from a mutualist to a pathogen may occur because of a single genomic change in the endosymbiont. This implies that there must be constant selection on endosymbionts to control their densities. |
| first_indexed | 2024-12-20T00:56:02Z |
| format | Article |
| id | doaj.art-eafda39b33004ab2b2d89a154e0cca97 |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-12-20T00:56:02Z |
| publishDate | 2015-02-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-eafda39b33004ab2b2d89a154e0cca972022-12-21T19:59:06ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852015-02-01132e100206510.1371/journal.pbio.1002065Mutualism breakdown by amplification of Wolbachia genes.Ewa ChrostekLuis TeixeiraMost insect species are associated with vertically transmitted endosymbionts. Because of the mode of transmission, the fitness of these symbionts is dependent on the fitness of the hosts. Therefore, these endosymbionts need to control their proliferation in order to minimize their cost for the host. The genetic bases and mechanisms of this regulation remain largely undetermined. The maternally inherited bacteria of the genus Wolbachia are the most common endosymbionts of insects, providing some of them with fitness benefits. In Drosophila melanogaster, Wolbachia wMelPop is a unique virulent variant that proliferates massively in the hosts and shortens their lifespan. The genetic bases of wMelPop virulence are unknown, and their identification would allow a better understanding of how Wolbachia levels are regulated. Here we show that amplification of a region containing eight Wolbachia genes, called Octomom, is responsible for wMelPop virulence. Using Drosophila lines selected for carrying Wolbachia with different Octomom copy numbers, we demonstrate that the number of Octomom copies determines Wolbachia titers and the strength of the lethal phenotype. Octomom amplification is unstable, and reversion of copy number to one reverts all the phenotypes. Our results provide a link between genotype and phenotype in Wolbachia and identify a genomic region regulating Wolbachia proliferation. We also prove that these bacteria can evolve rapidly. Rapid evolution by changes in gene copy number may be common in endosymbionts with a high number of mobile elements and other repeated regions. Understanding wMelPop pathogenicity and variability also allows researchers to better control and predict the outcome of releasing mosquitoes transinfected with this variant to block human vector-borne diseases. Our results show that transition from a mutualist to a pathogen may occur because of a single genomic change in the endosymbiont. This implies that there must be constant selection on endosymbionts to control their densities.https://doi.org/10.1371/journal.pbio.1002065 |
| spellingShingle | Ewa Chrostek Luis Teixeira Mutualism breakdown by amplification of Wolbachia genes. PLoS Biology |
| title | Mutualism breakdown by amplification of Wolbachia genes. |
| title_full | Mutualism breakdown by amplification of Wolbachia genes. |
| title_fullStr | Mutualism breakdown by amplification of Wolbachia genes. |
| title_full_unstemmed | Mutualism breakdown by amplification of Wolbachia genes. |
| title_short | Mutualism breakdown by amplification of Wolbachia genes. |
| title_sort | mutualism breakdown by amplification of wolbachia genes |
| url | https://doi.org/10.1371/journal.pbio.1002065 |
| work_keys_str_mv | AT ewachrostek mutualismbreakdownbyamplificationofwolbachiagenes AT luisteixeira mutualismbreakdownbyamplificationofwolbachiagenes |