The LacI-Family Transcription Factor, RbsR, is a Pleiotropic Regulator of Motility, Virulence, Siderophore and Antibiotic Production, Gas Vesicle Morphogenesis and Flotation in Serratia

Gas vesicles (GVs) are proteinaceous, gas-filled organelles used by some bacteria to enable upward movement into favorable air/liquid interfaces in aquatic environments. Serratia sp. ATCC39006 (S39006) was the first enterobacterium discovered to produce GVs naturally. The regulation of GV assembly...

Full description

Bibliographic Details
Main Authors: Lee, Chin Mei, Monson, Rita E., Adams, Rachel M., Salmond, George P. C.
Format: Article
Language:English
Published: Frontiers Media 2017
Subjects:
Online Access:http://umpir.ump.edu.my/id/eprint/18721/1/fmicb-08-01678.pdf
_version_ 1825823920199041024
author Lee, Chin Mei
Monson, Rita E.
Adams, Rachel M.
Salmond, George P. C.
author_facet Lee, Chin Mei
Monson, Rita E.
Adams, Rachel M.
Salmond, George P. C.
author_sort Lee, Chin Mei
collection UMP
description Gas vesicles (GVs) are proteinaceous, gas-filled organelles used by some bacteria to enable upward movement into favorable air/liquid interfaces in aquatic environments. Serratia sp. ATCC39006 (S39006) was the first enterobacterium discovered to produce GVs naturally. The regulation of GV assembly in this host is complex and part of a wider regulatory network affecting various phenotypes, including antibiotic biosynthesis. To identify new regulators of GVs, a comprehensive mutant library containing 71,000 insertion mutants was generated by random transposon mutagenesis and 311 putative GV-defectivemutants identified. Three of thesemutants were found to have a transposon inserted in a LacI family transcription regulator gene (rbsR) of the putative ribose operon. Each of these rbsR mutants was GV-defective; no GVs were visible by phase contrast microscopy (PCM) or transmission electron microscopy (TEM). GV deficiency was caused by the reduction of gvpA1 and gvrA transcription (the first genes of the two contiguous operons in the GV gene locus). Our results also showed that a mutation in rbsR was highly pleiotropic; the production of two secondary metabolites (carbapenem and prodigiosin antibiotics) was abolished. Interestingly, the intrinsic resistance to the carbapenem antibiotic was not affected by the rbsR mutation. In addition, the production of a siderophore, cellulase and plant virulence was reduced in the mutant, whereas it exhibited increased swimming and swarming motility. The RbsR protein was predicted to bind to regions upstreamof at least 18 genes in S39006 including rbsD (the first gene of the ribose operon) and gvrA. Electrophoretic mobility shift assays (EMSA) confirmed that RbsR bound to DNA sequences upstream of rbsD, but not gvrA. The results of this study indicate that RbsR is a global regulator that affects the modulation of GV biogenesis, but also with complex pleiotropic physiological impacts in S39006.
first_indexed 2024-03-06T12:18:17Z
format Article
id UMPir18721
institution Universiti Malaysia Pahang
language English
last_indexed 2024-03-06T12:18:17Z
publishDate 2017
publisher Frontiers Media
record_format dspace
spelling UMPir187212018-01-23T01:56:53Z http://umpir.ump.edu.my/id/eprint/18721/ The LacI-Family Transcription Factor, RbsR, is a Pleiotropic Regulator of Motility, Virulence, Siderophore and Antibiotic Production, Gas Vesicle Morphogenesis and Flotation in Serratia Lee, Chin Mei Monson, Rita E. Adams, Rachel M. Salmond, George P. C. QR Microbiology Gas vesicles (GVs) are proteinaceous, gas-filled organelles used by some bacteria to enable upward movement into favorable air/liquid interfaces in aquatic environments. Serratia sp. ATCC39006 (S39006) was the first enterobacterium discovered to produce GVs naturally. The regulation of GV assembly in this host is complex and part of a wider regulatory network affecting various phenotypes, including antibiotic biosynthesis. To identify new regulators of GVs, a comprehensive mutant library containing 71,000 insertion mutants was generated by random transposon mutagenesis and 311 putative GV-defectivemutants identified. Three of thesemutants were found to have a transposon inserted in a LacI family transcription regulator gene (rbsR) of the putative ribose operon. Each of these rbsR mutants was GV-defective; no GVs were visible by phase contrast microscopy (PCM) or transmission electron microscopy (TEM). GV deficiency was caused by the reduction of gvpA1 and gvrA transcription (the first genes of the two contiguous operons in the GV gene locus). Our results also showed that a mutation in rbsR was highly pleiotropic; the production of two secondary metabolites (carbapenem and prodigiosin antibiotics) was abolished. Interestingly, the intrinsic resistance to the carbapenem antibiotic was not affected by the rbsR mutation. In addition, the production of a siderophore, cellulase and plant virulence was reduced in the mutant, whereas it exhibited increased swimming and swarming motility. The RbsR protein was predicted to bind to regions upstreamof at least 18 genes in S39006 including rbsD (the first gene of the ribose operon) and gvrA. Electrophoretic mobility shift assays (EMSA) confirmed that RbsR bound to DNA sequences upstream of rbsD, but not gvrA. The results of this study indicate that RbsR is a global regulator that affects the modulation of GV biogenesis, but also with complex pleiotropic physiological impacts in S39006. Frontiers Media 2017 Article PeerReviewed application/pdf en cc_by http://umpir.ump.edu.my/id/eprint/18721/1/fmicb-08-01678.pdf Lee, Chin Mei and Monson, Rita E. and Adams, Rachel M. and Salmond, George P. C. (2017) The LacI-Family Transcription Factor, RbsR, is a Pleiotropic Regulator of Motility, Virulence, Siderophore and Antibiotic Production, Gas Vesicle Morphogenesis and Flotation in Serratia. Frontiers in Microbiology, 8. pp. 1-14. ISSN 1664-302X. (Published) https://doi.org/10.3389/fmicb.2017.01678 doi: 10.3389/fmicb.2017.01678
spellingShingle QR Microbiology
Lee, Chin Mei
Monson, Rita E.
Adams, Rachel M.
Salmond, George P. C.
The LacI-Family Transcription Factor, RbsR, is a Pleiotropic Regulator of Motility, Virulence, Siderophore and Antibiotic Production, Gas Vesicle Morphogenesis and Flotation in Serratia
title The LacI-Family Transcription Factor, RbsR, is a Pleiotropic Regulator of Motility, Virulence, Siderophore and Antibiotic Production, Gas Vesicle Morphogenesis and Flotation in Serratia
title_full The LacI-Family Transcription Factor, RbsR, is a Pleiotropic Regulator of Motility, Virulence, Siderophore and Antibiotic Production, Gas Vesicle Morphogenesis and Flotation in Serratia
title_fullStr The LacI-Family Transcription Factor, RbsR, is a Pleiotropic Regulator of Motility, Virulence, Siderophore and Antibiotic Production, Gas Vesicle Morphogenesis and Flotation in Serratia
title_full_unstemmed The LacI-Family Transcription Factor, RbsR, is a Pleiotropic Regulator of Motility, Virulence, Siderophore and Antibiotic Production, Gas Vesicle Morphogenesis and Flotation in Serratia
title_short The LacI-Family Transcription Factor, RbsR, is a Pleiotropic Regulator of Motility, Virulence, Siderophore and Antibiotic Production, Gas Vesicle Morphogenesis and Flotation in Serratia
title_sort laci family transcription factor rbsr is a pleiotropic regulator of motility virulence siderophore and antibiotic production gas vesicle morphogenesis and flotation in serratia
topic QR Microbiology
url http://umpir.ump.edu.my/id/eprint/18721/1/fmicb-08-01678.pdf
work_keys_str_mv AT leechinmei thelacifamilytranscriptionfactorrbsrisapleiotropicregulatorofmotilityvirulencesiderophoreandantibioticproductiongasvesiclemorphogenesisandflotationinserratia
AT monsonritae thelacifamilytranscriptionfactorrbsrisapleiotropicregulatorofmotilityvirulencesiderophoreandantibioticproductiongasvesiclemorphogenesisandflotationinserratia
AT adamsrachelm thelacifamilytranscriptionfactorrbsrisapleiotropicregulatorofmotilityvirulencesiderophoreandantibioticproductiongasvesiclemorphogenesisandflotationinserratia
AT salmondgeorgepc thelacifamilytranscriptionfactorrbsrisapleiotropicregulatorofmotilityvirulencesiderophoreandantibioticproductiongasvesiclemorphogenesisandflotationinserratia
AT leechinmei lacifamilytranscriptionfactorrbsrisapleiotropicregulatorofmotilityvirulencesiderophoreandantibioticproductiongasvesiclemorphogenesisandflotationinserratia
AT monsonritae lacifamilytranscriptionfactorrbsrisapleiotropicregulatorofmotilityvirulencesiderophoreandantibioticproductiongasvesiclemorphogenesisandflotationinserratia
AT adamsrachelm lacifamilytranscriptionfactorrbsrisapleiotropicregulatorofmotilityvirulencesiderophoreandantibioticproductiongasvesiclemorphogenesisandflotationinserratia
AT salmondgeorgepc lacifamilytranscriptionfactorrbsrisapleiotropicregulatorofmotilityvirulencesiderophoreandantibioticproductiongasvesiclemorphogenesisandflotationinserratia