Coordinated regulation of core and accessory genes in the multipartite genome of Sinorhizobium fredii.

Prokaryotes benefit from having accessory genes, but it is unclear how accessory genes can be linked with the core regulatory network when developing adaptations to new niches. Here we determined hierarchical core/accessory subsets in the multipartite pangenome (composed of genes from the chromosome...

Full description

Bibliographic Details
Main Authors: Jian Jiao, Meng Ni, Biliang Zhang, Ziding Zhang, J Peter W Young, Ting-Fung Chan, Wen Xin Chen, Hon-Ming Lam, Chang Fu Tian
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2018-05-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC5991415?pdf=render
_version_ 1818179164140732416
author Jian Jiao
Meng Ni
Biliang Zhang
Ziding Zhang
J Peter W Young
Ting-Fung Chan
Wen Xin Chen
Hon-Ming Lam
Chang Fu Tian
author_facet Jian Jiao
Meng Ni
Biliang Zhang
Ziding Zhang
J Peter W Young
Ting-Fung Chan
Wen Xin Chen
Hon-Ming Lam
Chang Fu Tian
author_sort Jian Jiao
collection DOAJ
description Prokaryotes benefit from having accessory genes, but it is unclear how accessory genes can be linked with the core regulatory network when developing adaptations to new niches. Here we determined hierarchical core/accessory subsets in the multipartite pangenome (composed of genes from the chromosome, chromid and plasmids) of the soybean microsymbiont Sinorhizobium fredii by comparing twelve Sinorhizobium genomes. Transcriptomes of two S. fredii strains at mid-log and stationary growth phases and in symbiotic conditions were obtained. The average level of gene expression, variation of expression between different conditions, and gene connectivity within the co-expression network were positively correlated with the gene conservation level from strain-specific accessory genes to genus core. Condition-dependent transcriptomes exhibited adaptive transcriptional changes in pangenome subsets shared by the two strains, while strain-dependent transcriptomes were enriched with accessory genes on the chromid. Proportionally more chromid genes than plasmid genes were co-expressed with chromosomal genes, while plasmid genes had a higher within-replicon connectivity in expression than chromid ones. However, key nitrogen fixation genes on the symbiosis plasmid were characterized by high connectivity in both within- and between-replicon analyses. Among those genes with host-specific upregulation patterns, chromosomal znu and mdt operons, encoding a conserved high-affinity zinc transporter and an accessory multi-drug efflux system, respectively, were experimentally demonstrated to be involved in host-specific symbiotic adaptation. These findings highlight the importance of integrative regulation of hierarchical core/accessory components in the multipartite genome of bacteria during niche adaptation and in shaping the prokaryotic pangenome in the long run.
first_indexed 2024-12-11T20:59:31Z
format Article
id doaj.art-6a0c93bd3a7b41ed859b91100c9123dd
institution Directory Open Access Journal
issn 1553-7390
1553-7404
language English
last_indexed 2024-12-11T20:59:31Z
publishDate 2018-05-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Genetics
spelling doaj.art-6a0c93bd3a7b41ed859b91100c9123dd2022-12-22T00:51:01ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042018-05-01145e100742810.1371/journal.pgen.1007428Coordinated regulation of core and accessory genes in the multipartite genome of Sinorhizobium fredii.Jian JiaoMeng NiBiliang ZhangZiding ZhangJ Peter W YoungTing-Fung ChanWen Xin ChenHon-Ming LamChang Fu TianProkaryotes benefit from having accessory genes, but it is unclear how accessory genes can be linked with the core regulatory network when developing adaptations to new niches. Here we determined hierarchical core/accessory subsets in the multipartite pangenome (composed of genes from the chromosome, chromid and plasmids) of the soybean microsymbiont Sinorhizobium fredii by comparing twelve Sinorhizobium genomes. Transcriptomes of two S. fredii strains at mid-log and stationary growth phases and in symbiotic conditions were obtained. The average level of gene expression, variation of expression between different conditions, and gene connectivity within the co-expression network were positively correlated with the gene conservation level from strain-specific accessory genes to genus core. Condition-dependent transcriptomes exhibited adaptive transcriptional changes in pangenome subsets shared by the two strains, while strain-dependent transcriptomes were enriched with accessory genes on the chromid. Proportionally more chromid genes than plasmid genes were co-expressed with chromosomal genes, while plasmid genes had a higher within-replicon connectivity in expression than chromid ones. However, key nitrogen fixation genes on the symbiosis plasmid were characterized by high connectivity in both within- and between-replicon analyses. Among those genes with host-specific upregulation patterns, chromosomal znu and mdt operons, encoding a conserved high-affinity zinc transporter and an accessory multi-drug efflux system, respectively, were experimentally demonstrated to be involved in host-specific symbiotic adaptation. These findings highlight the importance of integrative regulation of hierarchical core/accessory components in the multipartite genome of bacteria during niche adaptation and in shaping the prokaryotic pangenome in the long run.http://europepmc.org/articles/PMC5991415?pdf=render
spellingShingle Jian Jiao
Meng Ni
Biliang Zhang
Ziding Zhang
J Peter W Young
Ting-Fung Chan
Wen Xin Chen
Hon-Ming Lam
Chang Fu Tian
Coordinated regulation of core and accessory genes in the multipartite genome of Sinorhizobium fredii.
PLoS Genetics
title Coordinated regulation of core and accessory genes in the multipartite genome of Sinorhizobium fredii.
title_full Coordinated regulation of core and accessory genes in the multipartite genome of Sinorhizobium fredii.
title_fullStr Coordinated regulation of core and accessory genes in the multipartite genome of Sinorhizobium fredii.
title_full_unstemmed Coordinated regulation of core and accessory genes in the multipartite genome of Sinorhizobium fredii.
title_short Coordinated regulation of core and accessory genes in the multipartite genome of Sinorhizobium fredii.
title_sort coordinated regulation of core and accessory genes in the multipartite genome of sinorhizobium fredii
url http://europepmc.org/articles/PMC5991415?pdf=render
work_keys_str_mv AT jianjiao coordinatedregulationofcoreandaccessorygenesinthemultipartitegenomeofsinorhizobiumfredii
AT mengni coordinatedregulationofcoreandaccessorygenesinthemultipartitegenomeofsinorhizobiumfredii
AT biliangzhang coordinatedregulationofcoreandaccessorygenesinthemultipartitegenomeofsinorhizobiumfredii
AT zidingzhang coordinatedregulationofcoreandaccessorygenesinthemultipartitegenomeofsinorhizobiumfredii
AT jpeterwyoung coordinatedregulationofcoreandaccessorygenesinthemultipartitegenomeofsinorhizobiumfredii
AT tingfungchan coordinatedregulationofcoreandaccessorygenesinthemultipartitegenomeofsinorhizobiumfredii
AT wenxinchen coordinatedregulationofcoreandaccessorygenesinthemultipartitegenomeofsinorhizobiumfredii
AT honminglam coordinatedregulationofcoreandaccessorygenesinthemultipartitegenomeofsinorhizobiumfredii
AT changfutian coordinatedregulationofcoreandaccessorygenesinthemultipartitegenomeofsinorhizobiumfredii