Epistasis, core-genome disharmony, and adaptation in recombining bacteria
<p>Recombination of short DNA fragments via horizontal gene transfer (HGT) can introduce beneficial alleles, create genomic disharmony through negative epistasis, and create adaptive gene combinations through positive epistasis. For non-core (accessory) genes, the negative epistatic cost is li...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , |
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| Format: | Journal article |
| Language: | English |
| Published: |
American Society for Microbiology
2024
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| _version_ | 1811141209624674304 |
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| author | Taylor, AJ Yahara, K Pascoe, B Ko, S Mageiros, L Mourkas, E Calland, JK Puranen, S Hitchings, MD Jolley, KA Kobras, CM Bayliss, S Williams, NJ van Vliet, AHM Parkhill, J Maiden, MCJ Corander, J Hurst, LD Falush, D Keim, P Didelot, X Kelly, DJ Sheppard, SK |
| author_facet | Taylor, AJ Yahara, K Pascoe, B Ko, S Mageiros, L Mourkas, E Calland, JK Puranen, S Hitchings, MD Jolley, KA Kobras, CM Bayliss, S Williams, NJ van Vliet, AHM Parkhill, J Maiden, MCJ Corander, J Hurst, LD Falush, D Keim, P Didelot, X Kelly, DJ Sheppard, SK |
| author_sort | Taylor, AJ |
| collection | OXFORD |
| description | <p>Recombination of short DNA fragments via horizontal gene transfer (HGT) can introduce beneficial alleles, create genomic disharmony through negative epistasis, and create adaptive gene combinations through positive epistasis. For non-core (accessory) genes, the negative epistatic cost is likely to be minimal because the incoming genes have not co-evolved with the recipient genome and are frequently observed as tightly linked cassettes with major effects. By contrast, interspecific recombination in the core genome is expected to be rare because disruptive allelic replacement is likely to introduce negative epistasis. Why then is homologous recombination common in the core of bacterial genomes? To understand this enigma, we take advantage of an exceptional model system, the common enteric pathogens <em>Campylobacter jejuni</em> and <em>C. coli</em> that are known for very high magnitude interspecies gene flow in the core genome. As expected, HGT does indeed disrupt co-adapted allele pairings, indirect evidence of negative epistasis. However, multiple HGT events enable recovery of the genome’s co-adaption between introgressing alleles, even in core metabolism genes (e.g., formate dehydrogenase). These findings demonstrate that, even for complex traits, genetic coalitions can be decoupled, transferred, and independently reinstated in a new genetic background—facilitating transition between fitness peaks. In this example, the two-step recombinational process is associated with <em>C. coli</em> that are adapted to the agricultural niche.</p> |
| first_indexed | 2024-09-25T04:34:14Z |
| format | Journal article |
| id | oxford-uuid:ea54daa3-3700-4592-9905-e9f36edcacae |
| institution | University of Oxford |
| language | English |
| last_indexed | 2024-09-25T04:34:14Z |
| publishDate | 2024 |
| publisher | American Society for Microbiology |
| record_format | dspace |
| spelling | oxford-uuid:ea54daa3-3700-4592-9905-e9f36edcacae2024-09-05T14:48:18ZEpistasis, core-genome disharmony, and adaptation in recombining bacteriaJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:ea54daa3-3700-4592-9905-e9f36edcacaeEnglishSymplectic ElementsAmerican Society for Microbiology2024Taylor, AJYahara, KPascoe, BKo, SMageiros, LMourkas, ECalland, JKPuranen, SHitchings, MDJolley, KAKobras, CMBayliss, SWilliams, NJvan Vliet, AHMParkhill, JMaiden, MCJCorander, JHurst, LDFalush, DKeim, PDidelot, XKelly, DJSheppard, SK<p>Recombination of short DNA fragments via horizontal gene transfer (HGT) can introduce beneficial alleles, create genomic disharmony through negative epistasis, and create adaptive gene combinations through positive epistasis. For non-core (accessory) genes, the negative epistatic cost is likely to be minimal because the incoming genes have not co-evolved with the recipient genome and are frequently observed as tightly linked cassettes with major effects. By contrast, interspecific recombination in the core genome is expected to be rare because disruptive allelic replacement is likely to introduce negative epistasis. Why then is homologous recombination common in the core of bacterial genomes? To understand this enigma, we take advantage of an exceptional model system, the common enteric pathogens <em>Campylobacter jejuni</em> and <em>C. coli</em> that are known for very high magnitude interspecies gene flow in the core genome. As expected, HGT does indeed disrupt co-adapted allele pairings, indirect evidence of negative epistasis. However, multiple HGT events enable recovery of the genome’s co-adaption between introgressing alleles, even in core metabolism genes (e.g., formate dehydrogenase). These findings demonstrate that, even for complex traits, genetic coalitions can be decoupled, transferred, and independently reinstated in a new genetic background—facilitating transition between fitness peaks. In this example, the two-step recombinational process is associated with <em>C. coli</em> that are adapted to the agricultural niche.</p> |
| spellingShingle | Taylor, AJ Yahara, K Pascoe, B Ko, S Mageiros, L Mourkas, E Calland, JK Puranen, S Hitchings, MD Jolley, KA Kobras, CM Bayliss, S Williams, NJ van Vliet, AHM Parkhill, J Maiden, MCJ Corander, J Hurst, LD Falush, D Keim, P Didelot, X Kelly, DJ Sheppard, SK Epistasis, core-genome disharmony, and adaptation in recombining bacteria |
| title | Epistasis, core-genome disharmony, and adaptation in recombining bacteria |
| title_full | Epistasis, core-genome disharmony, and adaptation in recombining bacteria |
| title_fullStr | Epistasis, core-genome disharmony, and adaptation in recombining bacteria |
| title_full_unstemmed | Epistasis, core-genome disharmony, and adaptation in recombining bacteria |
| title_short | Epistasis, core-genome disharmony, and adaptation in recombining bacteria |
| title_sort | epistasis core genome disharmony and adaptation in recombining bacteria |
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