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Peer-reviewedCC BY 4.0Frontiers in Microbiology

Transcriptional silencing of a conjugative Sinorhizobium megaplasmid upon transfer to different rhizobial species

  1. 1Programa de Ingeniería Genómica, Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México
  2. 2Departamento de Ciencias Biológicas, Facultad de Ciencias Exactas, Instituto de Biotecnología y Biología Molecular (IBBM)—CCT CONICET—La Plata, Universidad Nacional de la Plata

Abstract

Horizontal gene transfer of large conjugative megaplasmids drives bacterial evolution, however, it forces new hosts to rapidly adapt to a massive influx of exogenous DNA; even the acquisition of small plasmids can have variable effects on host genome activity and fitness. In Sinorhizobium fredii GR64 (symbiont of the common bean) the megaplasmid pSfr64a (191 kb) displays a high conjugative transfer rate. Interestingly, when pSfr64a is transferred to Rhizobium etli (another bean symbiont) conjugative transfer from this host became nearly undetectable, whereas in Agrobacterium tumefaciens it is maintained at a high rate. To unravel the host-plasmid dynamics driving this host-specific response, we undertook a transcriptome analysis of pSfr64a in different hosts. The results reveal that in its original host, pSfr64a transcriptional activity is centered in four zones, including the conjugative zone. Expression of these zones is markedly quelled when pSfr64a resides in R. etli , explaining the reduction in conjugative activity. Crucially, this silencing ensures minimal effects on the host’s transcriptional activity, allowing R. etli to adapt to the megaplasmid with zero fitness cost. In contrast, a weak silencing in A. tumefaciens allows conjugation, but triggers a widespread transcriptional reorganization across both linear and circular chromosomes, severely penalizing host fitness. Although inactivation of the xenogeneic silencer MucR in R. etli leads to a partial recovery of plasmid expression, it does not restore conjugation. These results highlight a fundamental evolutionary conflict: the successful adaptation to a newly acquired megaplasmid depends on a hierarchical, host-specific silencing architecture that must tame the biological cost of the plasmid’s “selfish mode.”

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BibTeX
@article{cruz2026transcriptional,
  title = {{Transcriptional silencing of a conjugative Sinorhizobium megaplasmid upon transfer to different rhizobial species}},
  author = {Cristina de la Cruz and Laura Cervantes and Gonzalo Torres-Tejerizo and David Romero},
  journal = {Frontiers in Microbiology},
  year = {2026},
  month = oct,
  doi = {10.3389/fmicb.2026.1977405},
  url = {https://www.frontiersin.org/articles/10.3389/fmicb.2026.1977405/full},
  note = {CC BY 4.0},
}
RIS
TY  - JOUR
TI  - Transcriptional silencing of a conjugative Sinorhizobium megaplasmid upon transfer to different rhizobial species
AU  - Cristina de la Cruz
AU  - Laura Cervantes
AU  - Gonzalo Torres-Tejerizo
AU  - David Romero
PY  - 2026
DA  - 2026/10/22
JO  - Frontiers in Microbiology
DO  - 10.3389/fmicb.2026.1977405
UR  - https://www.frontiersin.org/articles/10.3389/fmicb.2026.1977405/full
AB  - Horizontal gene transfer of large conjugative megaplasmids drives bacterial evolution, however, it forces new hosts to rapidly adapt to a massive influx of exogenous DNA; even the acquisition of small plasmids can have variable effects on host genome activity and fitness. In Sinorhizobium fredii GR64 (symbiont of the common bean) the megaplasmid pSfr64a (191 kb) displays a high conjugative transfer rate. Interestingly, when pSfr64a is transferred to Rhizobium etli (another bean symbiont) conjugative transfer from this host became nearly undetectable, whereas in Agrobacterium tumefaciens it is maintained at a high rate. To unravel the host-plasmid dynamics driving this host-specific response, we undertook a transcriptome analysis of pSfr64a in different hosts. The results reveal that in its original host, pSfr64a transcriptional activity is centered in four zones, including the conjugative zone. Expression of these zones is markedly quelled when pSfr64a resides in R. etli , explaining the reduction in conjugative activity. Crucially, this silencing ensures minimal effects on the host’s transcriptional activity, allowing R. etli to adapt to the megaplasmid with zero fitness cost. In contrast, a weak silencing in A. tumefaciens allows conjugation, but triggers a widespread transcriptional reorganization across both linear and circular chromosomes, severely penalizing host fitness. Although inactivation of the xenogeneic silencer MucR in R. etli leads to a partial recovery of plasmid expression, it does not restore conjugation. These results highlight a fundamental evolutionary conflict: the successful adaptation to a newly acquired megaplasmid depends on a hierarchical, host-specific silencing architecture that must tame the biological cost of the plasmid’s “selfish mode.”
SN  - 1664-302X
ER  -