Rhomboids of Mycobacteria: characterization using an aarA mutant of Providencia stuartii and gene deletion in Mycobacterium smegmatis.

<h4>Background</h4>Rhomboids are ubiquitous proteins with unknown roles in mycobacteria. However, bioinformatics suggested putative roles in DNA replication pathways and metabolite transport. Here, mycobacterial rhomboid-encoding genes were characterized; first, using the Providencia stu...

Full description

Saved in:
Bibliographic Details
Main Authors: David Patrick Kateete, Fred Ashaba Katabazi, Alfred Okeng, Moses Okee, Conrad Musinguzi, Benon Byamugisha Asiimwe, Samuel Kyobe, Jeniffer Asiimwe, W Henry Boom, Moses Lutaakome Joloba
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0045741&type=printable
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850224863464128512
author David Patrick Kateete
Fred Ashaba Katabazi
Alfred Okeng
Moses Okee
Conrad Musinguzi
Benon Byamugisha Asiimwe
Samuel Kyobe
Jeniffer Asiimwe
W Henry Boom
Moses Lutaakome Joloba
author_facet David Patrick Kateete
Fred Ashaba Katabazi
Alfred Okeng
Moses Okee
Conrad Musinguzi
Benon Byamugisha Asiimwe
Samuel Kyobe
Jeniffer Asiimwe
W Henry Boom
Moses Lutaakome Joloba
author_sort David Patrick Kateete
collection DOAJ
description <h4>Background</h4>Rhomboids are ubiquitous proteins with unknown roles in mycobacteria. However, bioinformatics suggested putative roles in DNA replication pathways and metabolite transport. Here, mycobacterial rhomboid-encoding genes were characterized; first, using the Providencia stuartii null-rhomboid mutant and then deleted from Mycobacterium smegmatis for additional insight in mycobacteria.<h4>Methodology/principal findings</h4>Using in silico analysis we identified in M. tuberculosis genome the genes encoding two putative rhomboid proteins; Rv0110 (referred to as "rhomboid protease 1") and Rv1337 ("rhomboid protease 2"). Genes encoding orthologs of these proteins are widely represented in all mycobacterial species. When transformed into P. stuartii null-rhomboid mutant (ΔaarA), genes encoding mycobacterial orthologs of "rhomboid protease 2" fully restored AarA activity (AarA is the rhomboid protein of P. stuartii). However, most genes encoding mycobacterial "rhomboid protease 1" orthologs did not. Furthermore, upon gene deletion in M. smegmatis, the ΔMSMEG_4904 single mutant (which lost the gene encoding MSMEG_4904, orthologous to Rv1337, "rhomboid protease 2") formed the least biofilms and was also more susceptible to ciprofloxacin and novobiocin, antimicrobials that inhibit DNA gyrase. However, the ΔMSMEG_5036 single mutant (which lost the gene encoding MSMEG_5036, orthologous to Rv0110, "rhomboid protease 1") was not as susceptible. Surprisingly, the double rhomboid mutant ΔMSMEG_4904-ΔMSMEG_5036 (which lost genes encoding both homologs) was also not as susceptible suggesting compensatory effects following deletion of both rhomboid-encoding genes. Indeed, transforming the double mutant with a plasmid encoding MSMEG_5036 produced phenotypes of the ΔMSMEG_4904 single mutant (i.e. susceptibility to ciprofloxacin and novobiocin).<h4>Conclusions/significance</h4>Mycobacterial rhomboid-encoding genes exhibit differences in complementing aarA whereby it's only genes encoding "rhomboid protease 2" orthologs that fully restore AarA activity. Additionally, gene deletion data suggests inhibition of DNA gyrase by MSMEG_4904; however, the ameliorated effect in the double mutant suggests occurrence of compensatory mechanisms following deletion of genes encoding both rhomboids.
format Article
id doaj-art-76174808fa9a4adcb0aa9deee380dbbc
institution OA Journals
issn 1932-6203
language English
publishDate 2012-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj-art-76174808fa9a4adcb0aa9deee380dbbc2025-08-20T02:05:31ZengPublic Library of Science (PLoS)PLoS ONE1932-62032012-01-0179e4574110.1371/journal.pone.0045741Rhomboids of Mycobacteria: characterization using an aarA mutant of Providencia stuartii and gene deletion in Mycobacterium smegmatis.David Patrick KateeteFred Ashaba KatabaziAlfred OkengMoses OkeeConrad MusinguziBenon Byamugisha AsiimweSamuel KyobeJeniffer AsiimweW Henry BoomMoses Lutaakome Joloba<h4>Background</h4>Rhomboids are ubiquitous proteins with unknown roles in mycobacteria. However, bioinformatics suggested putative roles in DNA replication pathways and metabolite transport. Here, mycobacterial rhomboid-encoding genes were characterized; first, using the Providencia stuartii null-rhomboid mutant and then deleted from Mycobacterium smegmatis for additional insight in mycobacteria.<h4>Methodology/principal findings</h4>Using in silico analysis we identified in M. tuberculosis genome the genes encoding two putative rhomboid proteins; Rv0110 (referred to as "rhomboid protease 1") and Rv1337 ("rhomboid protease 2"). Genes encoding orthologs of these proteins are widely represented in all mycobacterial species. When transformed into P. stuartii null-rhomboid mutant (ΔaarA), genes encoding mycobacterial orthologs of "rhomboid protease 2" fully restored AarA activity (AarA is the rhomboid protein of P. stuartii). However, most genes encoding mycobacterial "rhomboid protease 1" orthologs did not. Furthermore, upon gene deletion in M. smegmatis, the ΔMSMEG_4904 single mutant (which lost the gene encoding MSMEG_4904, orthologous to Rv1337, "rhomboid protease 2") formed the least biofilms and was also more susceptible to ciprofloxacin and novobiocin, antimicrobials that inhibit DNA gyrase. However, the ΔMSMEG_5036 single mutant (which lost the gene encoding MSMEG_5036, orthologous to Rv0110, "rhomboid protease 1") was not as susceptible. Surprisingly, the double rhomboid mutant ΔMSMEG_4904-ΔMSMEG_5036 (which lost genes encoding both homologs) was also not as susceptible suggesting compensatory effects following deletion of both rhomboid-encoding genes. Indeed, transforming the double mutant with a plasmid encoding MSMEG_5036 produced phenotypes of the ΔMSMEG_4904 single mutant (i.e. susceptibility to ciprofloxacin and novobiocin).<h4>Conclusions/significance</h4>Mycobacterial rhomboid-encoding genes exhibit differences in complementing aarA whereby it's only genes encoding "rhomboid protease 2" orthologs that fully restore AarA activity. Additionally, gene deletion data suggests inhibition of DNA gyrase by MSMEG_4904; however, the ameliorated effect in the double mutant suggests occurrence of compensatory mechanisms following deletion of genes encoding both rhomboids.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0045741&type=printable
spellingShingle David Patrick Kateete
Fred Ashaba Katabazi
Alfred Okeng
Moses Okee
Conrad Musinguzi
Benon Byamugisha Asiimwe
Samuel Kyobe
Jeniffer Asiimwe
W Henry Boom
Moses Lutaakome Joloba
Rhomboids of Mycobacteria: characterization using an aarA mutant of Providencia stuartii and gene deletion in Mycobacterium smegmatis.
PLoS ONE
title Rhomboids of Mycobacteria: characterization using an aarA mutant of Providencia stuartii and gene deletion in Mycobacterium smegmatis.
title_full Rhomboids of Mycobacteria: characterization using an aarA mutant of Providencia stuartii and gene deletion in Mycobacterium smegmatis.
title_fullStr Rhomboids of Mycobacteria: characterization using an aarA mutant of Providencia stuartii and gene deletion in Mycobacterium smegmatis.
title_full_unstemmed Rhomboids of Mycobacteria: characterization using an aarA mutant of Providencia stuartii and gene deletion in Mycobacterium smegmatis.
title_short Rhomboids of Mycobacteria: characterization using an aarA mutant of Providencia stuartii and gene deletion in Mycobacterium smegmatis.
title_sort rhomboids of mycobacteria characterization using an aara mutant of providencia stuartii and gene deletion in mycobacterium smegmatis
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0045741&type=printable
work_keys_str_mv AT davidpatrickkateete rhomboidsofmycobacteriacharacterizationusinganaaramutantofprovidenciastuartiiandgenedeletioninmycobacteriumsmegmatis
AT fredashabakatabazi rhomboidsofmycobacteriacharacterizationusinganaaramutantofprovidenciastuartiiandgenedeletioninmycobacteriumsmegmatis
AT alfredokeng rhomboidsofmycobacteriacharacterizationusinganaaramutantofprovidenciastuartiiandgenedeletioninmycobacteriumsmegmatis
AT mosesokee rhomboidsofmycobacteriacharacterizationusinganaaramutantofprovidenciastuartiiandgenedeletioninmycobacteriumsmegmatis
AT conradmusinguzi rhomboidsofmycobacteriacharacterizationusinganaaramutantofprovidenciastuartiiandgenedeletioninmycobacteriumsmegmatis
AT benonbyamugishaasiimwe rhomboidsofmycobacteriacharacterizationusinganaaramutantofprovidenciastuartiiandgenedeletioninmycobacteriumsmegmatis
AT samuelkyobe rhomboidsofmycobacteriacharacterizationusinganaaramutantofprovidenciastuartiiandgenedeletioninmycobacteriumsmegmatis
AT jenifferasiimwe rhomboidsofmycobacteriacharacterizationusinganaaramutantofprovidenciastuartiiandgenedeletioninmycobacteriumsmegmatis
AT whenryboom rhomboidsofmycobacteriacharacterizationusinganaaramutantofprovidenciastuartiiandgenedeletioninmycobacteriumsmegmatis
AT moseslutaakomejoloba rhomboidsofmycobacteriacharacterizationusinganaaramutantofprovidenciastuartiiandgenedeletioninmycobacteriumsmegmatis