Mutational features of chromids and chromosomes in Pseudoalteromonas provide new insights into the evolution of secondary replicons

ABSTRACT The genomes of multi-replicon bacteria are composed of a primary replicon (the chromosome) and secondary replicons (chromids). Currently, there is a lack of understanding of the mutation features and evolutionary patterns of these different replicons. Specifically, in the genus Pseudoaltero...

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Main Authors: Wanyue Jiang, Jiao Pan, Tongtong Lin, Yaohai Wang, Yanze Wang, Rongxiao Zhang, Xiaoming Zhou, Yu Zhang
Format: Article
Language:English
Published: American Society for Microbiology 2025-05-01
Series:Microbiology Spectrum
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Online Access:https://journals.asm.org/doi/10.1128/spectrum.02127-24
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author Wanyue Jiang
Jiao Pan
Tongtong Lin
Yaohai Wang
Yanze Wang
Rongxiao Zhang
Xiaoming Zhou
Yu Zhang
author_facet Wanyue Jiang
Jiao Pan
Tongtong Lin
Yaohai Wang
Yanze Wang
Rongxiao Zhang
Xiaoming Zhou
Yu Zhang
author_sort Wanyue Jiang
collection DOAJ
description ABSTRACT The genomes of multi-replicon bacteria are composed of a primary replicon (the chromosome) and secondary replicons (chromids). Currently, there is a lack of understanding of the mutation features and evolutionary patterns of these different replicons. Specifically, in the genus Pseudoalteromonas, the chromids of multi-replicon species exhibit both unidirectional and bidirectional replication. Here, we investigated the similarities and differences between chromosomes and chromids in sequence composition and gene synteny of Pseudoalteromonas species by comparative genomic analysis, as well as the spontaneous mutation features of different replicons by mutation accumulation (MA) experiments combined with whole-genome sequencing strategy (MA-WGS). MA-WGS analysis revealed that there was no significant difference between chromids and chromosomes in the mutation rate or mutation spectrum of P. sp. LC0214 (where the chromid is unidirectional in replication) and P. sp. JCM12884T (where the chromid is bidirectional in replication). In addition, the context-dependence and variation pattern of the base-pair substitutions (BPSs) rates of the entire replicons exhibited differences that may be caused by the different replication directions of the chromids. The results of this study provide a new theoretical foundation for an in-depth understanding of the origin and evolution of chromids in multi-replicon bacterial species and facilitate further exploration of the complex mechanisms of bacterial diversity.IMPORTANCEDe novo mutations are a critical driving force in species evolution. Currently, there is a lack of sufficient research on the influence of replicon types on the occurrence of genomic mutations in bacteria. Moreover, the scarcity in systematic analysis and comparison of spontaneous mutation features between different replicons results in the limited information on the evolutionary dynamics of multi-replicon species. The diversity of replication direction in the multi-replicon species of the genus Pseudoalteromonas provides a unique opportunity for studying the impact of replication direction on the patterns of mutation. In addition to the composition characteristics between chromosomes and chromids, the spontaneous mutation rates in the context-dependence and variation pattern of the base-pair substitutions (BPSs) across different replicons within Pseudoalteromonas species revealed in this study provide valuable insights into the evolutionary dynamics of bacterial secondary replicons.
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spelling doaj-art-c3ed364b6a394cd199a5a667931b1f222025-08-20T03:11:48ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972025-05-0113510.1128/spectrum.02127-24Mutational features of chromids and chromosomes in Pseudoalteromonas provide new insights into the evolution of secondary repliconsWanyue Jiang0Jiao Pan1Tongtong Lin2Yaohai Wang3Yanze Wang4Rongxiao Zhang5Xiaoming Zhou6Yu Zhang7Key Laboratory of Evolution and Marine Biodiversity (Ministry of Education), Institute of Evolution and Marine Biodiversity, KLMME, Ocean University of China, Qingdao, Shandong, ChinaKey Laboratory of Evolution and Marine Biodiversity (Ministry of Education), Institute of Evolution and Marine Biodiversity, KLMME, Ocean University of China, Qingdao, Shandong, ChinaKey Laboratory of Evolution and Marine Biodiversity (Ministry of Education), Institute of Evolution and Marine Biodiversity, KLMME, Ocean University of China, Qingdao, Shandong, ChinaKey Laboratory of Evolution and Marine Biodiversity (Ministry of Education), Institute of Evolution and Marine Biodiversity, KLMME, Ocean University of China, Qingdao, Shandong, ChinaKey Laboratory of Evolution and Marine Biodiversity (Ministry of Education), Institute of Evolution and Marine Biodiversity, KLMME, Ocean University of China, Qingdao, Shandong, ChinaKey Laboratory of Evolution and Marine Biodiversity (Ministry of Education), Institute of Evolution and Marine Biodiversity, KLMME, Ocean University of China, Qingdao, Shandong, ChinaKey Laboratory of Evolution and Marine Biodiversity (Ministry of Education), Institute of Evolution and Marine Biodiversity, KLMME, Ocean University of China, Qingdao, Shandong, ChinaKey Laboratory of Evolution and Marine Biodiversity (Ministry of Education), Institute of Evolution and Marine Biodiversity, KLMME, Ocean University of China, Qingdao, Shandong, ChinaABSTRACT The genomes of multi-replicon bacteria are composed of a primary replicon (the chromosome) and secondary replicons (chromids). Currently, there is a lack of understanding of the mutation features and evolutionary patterns of these different replicons. Specifically, in the genus Pseudoalteromonas, the chromids of multi-replicon species exhibit both unidirectional and bidirectional replication. Here, we investigated the similarities and differences between chromosomes and chromids in sequence composition and gene synteny of Pseudoalteromonas species by comparative genomic analysis, as well as the spontaneous mutation features of different replicons by mutation accumulation (MA) experiments combined with whole-genome sequencing strategy (MA-WGS). MA-WGS analysis revealed that there was no significant difference between chromids and chromosomes in the mutation rate or mutation spectrum of P. sp. LC0214 (where the chromid is unidirectional in replication) and P. sp. JCM12884T (where the chromid is bidirectional in replication). In addition, the context-dependence and variation pattern of the base-pair substitutions (BPSs) rates of the entire replicons exhibited differences that may be caused by the different replication directions of the chromids. The results of this study provide a new theoretical foundation for an in-depth understanding of the origin and evolution of chromids in multi-replicon bacterial species and facilitate further exploration of the complex mechanisms of bacterial diversity.IMPORTANCEDe novo mutations are a critical driving force in species evolution. Currently, there is a lack of sufficient research on the influence of replicon types on the occurrence of genomic mutations in bacteria. Moreover, the scarcity in systematic analysis and comparison of spontaneous mutation features between different replicons results in the limited information on the evolutionary dynamics of multi-replicon species. The diversity of replication direction in the multi-replicon species of the genus Pseudoalteromonas provides a unique opportunity for studying the impact of replication direction on the patterns of mutation. In addition to the composition characteristics between chromosomes and chromids, the spontaneous mutation rates in the context-dependence and variation pattern of the base-pair substitutions (BPSs) across different replicons within Pseudoalteromonas species revealed in this study provide valuable insights into the evolutionary dynamics of bacterial secondary replicons.https://journals.asm.org/doi/10.1128/spectrum.02127-24multi-repliconmutation featuresreplication directionchromid evolutionPseudoalteromonas
spellingShingle Wanyue Jiang
Jiao Pan
Tongtong Lin
Yaohai Wang
Yanze Wang
Rongxiao Zhang
Xiaoming Zhou
Yu Zhang
Mutational features of chromids and chromosomes in Pseudoalteromonas provide new insights into the evolution of secondary replicons
Microbiology Spectrum
multi-replicon
mutation features
replication direction
chromid evolution
Pseudoalteromonas
title Mutational features of chromids and chromosomes in Pseudoalteromonas provide new insights into the evolution of secondary replicons
title_full Mutational features of chromids and chromosomes in Pseudoalteromonas provide new insights into the evolution of secondary replicons
title_fullStr Mutational features of chromids and chromosomes in Pseudoalteromonas provide new insights into the evolution of secondary replicons
title_full_unstemmed Mutational features of chromids and chromosomes in Pseudoalteromonas provide new insights into the evolution of secondary replicons
title_short Mutational features of chromids and chromosomes in Pseudoalteromonas provide new insights into the evolution of secondary replicons
title_sort mutational features of chromids and chromosomes in pseudoalteromonas provide new insights into the evolution of secondary replicons
topic multi-replicon
mutation features
replication direction
chromid evolution
Pseudoalteromonas
url https://journals.asm.org/doi/10.1128/spectrum.02127-24
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