Cargando…

Deciphering a unique biotin scavenging pathway with redundant genes in the probiotic bacterium Lactococcus lactis

Biotin protein ligase (BPL) is widespread in the three domains of the life. The paradigm BPL is the Escherichia coli BirA protein, which also functions as a repressor for the biotin biosynthesis pathway. Here we report that Lactococcus lactis possesses two different orthologues of birA (birA1(_LL) a...

Descripción completa

Detalles Bibliográficos
Autores principales: Zhang, Huimin, Wang, Qingjing, Fisher, Derek J., Cai, Mingzhu, Chakravartty, Vandana, Ye, Huiyan, Li, Ping, Solbiati, Jose O., Feng, Youjun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4861984/
https://www.ncbi.nlm.nih.gov/pubmed/27161258
http://dx.doi.org/10.1038/srep25680
_version_ 1782431290377633792
author Zhang, Huimin
Wang, Qingjing
Fisher, Derek J.
Cai, Mingzhu
Chakravartty, Vandana
Ye, Huiyan
Li, Ping
Solbiati, Jose O.
Feng, Youjun
author_facet Zhang, Huimin
Wang, Qingjing
Fisher, Derek J.
Cai, Mingzhu
Chakravartty, Vandana
Ye, Huiyan
Li, Ping
Solbiati, Jose O.
Feng, Youjun
author_sort Zhang, Huimin
collection PubMed
description Biotin protein ligase (BPL) is widespread in the three domains of the life. The paradigm BPL is the Escherichia coli BirA protein, which also functions as a repressor for the biotin biosynthesis pathway. Here we report that Lactococcus lactis possesses two different orthologues of birA (birA1(_LL) and birA2(_LL)). Unlike the scenario in E. coli, L. lactis appears to be auxotrophic for biotin in that it lacks a full biotin biosynthesis pathway. In contrast, it retains two biotin transporter-encoding genes (bioY1(_LL) and bioY2(_LL)), suggesting the use of a scavenging strategy to obtain biotin from the environment. The in vivo function of the two L. lactis birA genes was judged by their abilities to complement the conditional lethal E. coli birA mutant. Thin-layer chromatography and mass spectroscopy assays demonstrated that these two recombinant BirA proteins catalyze the biotinylation reaction of the acceptor biotin carboxyl carrier protein (BCCP), through the expected biotinoyl-AMP intermediate. Gel shift assays were used to characterize bioY1(_LL) and BirA1(_LL). We also determined the ability to uptake (3)H-biotin by L. lactis. Taken together, our results deciphered a unique biotin scavenging pathway with redundant genes present in the probiotic bacterium L. lactis.
format Online
Article
Text
id pubmed-4861984
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher Nature Publishing Group
record_format MEDLINE/PubMed
spelling pubmed-48619842016-05-23 Deciphering a unique biotin scavenging pathway with redundant genes in the probiotic bacterium Lactococcus lactis Zhang, Huimin Wang, Qingjing Fisher, Derek J. Cai, Mingzhu Chakravartty, Vandana Ye, Huiyan Li, Ping Solbiati, Jose O. Feng, Youjun Sci Rep Article Biotin protein ligase (BPL) is widespread in the three domains of the life. The paradigm BPL is the Escherichia coli BirA protein, which also functions as a repressor for the biotin biosynthesis pathway. Here we report that Lactococcus lactis possesses two different orthologues of birA (birA1(_LL) and birA2(_LL)). Unlike the scenario in E. coli, L. lactis appears to be auxotrophic for biotin in that it lacks a full biotin biosynthesis pathway. In contrast, it retains two biotin transporter-encoding genes (bioY1(_LL) and bioY2(_LL)), suggesting the use of a scavenging strategy to obtain biotin from the environment. The in vivo function of the two L. lactis birA genes was judged by their abilities to complement the conditional lethal E. coli birA mutant. Thin-layer chromatography and mass spectroscopy assays demonstrated that these two recombinant BirA proteins catalyze the biotinylation reaction of the acceptor biotin carboxyl carrier protein (BCCP), through the expected biotinoyl-AMP intermediate. Gel shift assays were used to characterize bioY1(_LL) and BirA1(_LL). We also determined the ability to uptake (3)H-biotin by L. lactis. Taken together, our results deciphered a unique biotin scavenging pathway with redundant genes present in the probiotic bacterium L. lactis. Nature Publishing Group 2016-05-10 /pmc/articles/PMC4861984/ /pubmed/27161258 http://dx.doi.org/10.1038/srep25680 Text en Copyright © 2016, Macmillan Publishers Limited http://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
spellingShingle Article
Zhang, Huimin
Wang, Qingjing
Fisher, Derek J.
Cai, Mingzhu
Chakravartty, Vandana
Ye, Huiyan
Li, Ping
Solbiati, Jose O.
Feng, Youjun
Deciphering a unique biotin scavenging pathway with redundant genes in the probiotic bacterium Lactococcus lactis
title Deciphering a unique biotin scavenging pathway with redundant genes in the probiotic bacterium Lactococcus lactis
title_full Deciphering a unique biotin scavenging pathway with redundant genes in the probiotic bacterium Lactococcus lactis
title_fullStr Deciphering a unique biotin scavenging pathway with redundant genes in the probiotic bacterium Lactococcus lactis
title_full_unstemmed Deciphering a unique biotin scavenging pathway with redundant genes in the probiotic bacterium Lactococcus lactis
title_short Deciphering a unique biotin scavenging pathway with redundant genes in the probiotic bacterium Lactococcus lactis
title_sort deciphering a unique biotin scavenging pathway with redundant genes in the probiotic bacterium lactococcus lactis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4861984/
https://www.ncbi.nlm.nih.gov/pubmed/27161258
http://dx.doi.org/10.1038/srep25680
work_keys_str_mv AT zhanghuimin decipheringauniquebiotinscavengingpathwaywithredundantgenesintheprobioticbacteriumlactococcuslactis
AT wangqingjing decipheringauniquebiotinscavengingpathwaywithredundantgenesintheprobioticbacteriumlactococcuslactis
AT fisherderekj decipheringauniquebiotinscavengingpathwaywithredundantgenesintheprobioticbacteriumlactococcuslactis
AT caimingzhu decipheringauniquebiotinscavengingpathwaywithredundantgenesintheprobioticbacteriumlactococcuslactis
AT chakravarttyvandana decipheringauniquebiotinscavengingpathwaywithredundantgenesintheprobioticbacteriumlactococcuslactis
AT yehuiyan decipheringauniquebiotinscavengingpathwaywithredundantgenesintheprobioticbacteriumlactococcuslactis
AT liping decipheringauniquebiotinscavengingpathwaywithredundantgenesintheprobioticbacteriumlactococcuslactis
AT solbiatijoseo decipheringauniquebiotinscavengingpathwaywithredundantgenesintheprobioticbacteriumlactococcuslactis
AT fengyoujun decipheringauniquebiotinscavengingpathwaywithredundantgenesintheprobioticbacteriumlactococcuslactis