Nucleoid Associated Proteins: The Small Organizers That Help to Cope With Stress

Hołówka, Joanna; Zakrzewska‐Czerwińska, Jolanta

doi:10.3389/fmicb.2020.00590

Cited by 84 publications

(84 citation statements)

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“…The lack of MSMEG_1060 or Lsr2 increases cell susceptibility to antibiotics. A growing body of evidence suggests that NAP-mediated adaptation strategies help bacteria endure unfavorable conditions, including exposure to antibiotics (6,32). Therefore, we sought to examine if MSMEG_1060 and Lsr2 proteins help M. smegmatis survive in the presence of antibiotics.…”

Section: Resultsmentioning

confidence: 99%

“…To grow and survive, the free-living soil bacterium must quickly adapt to changing environmental conditions, including exposure to various stresses. Among the many possible adaptation strategies, NAP-induced changes in chromosome organization resulting in physical protection of the DNA and/ or altered gene expression appear to be the most rapid adaptation strategies (6,19,32) The Dlsr2 M. smegmatis strain exhibits a number of morphological disorders that are related to changes in the outer membrane composition. Cells devoid of Lsr2 produce more LOSs (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Nucleoid-associated proteins (NAPs) organize the chromosomal structure and act as global transcription regulators (5). They are believed to play crucial roles in the ability of a bacterium to quickly adapt to unfavorable conditions, particularly under stress (6). By inducing topological and/or structural changes in DNA, they can affect the global transcription profile.…”

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Lsr2 and Its Novel Paralogue Mediate the Adjustment of Mycobacterium smegmatis to Unfavorable Environmental Conditions

Kołodziej

Łebkowski

Płociński

et al. 2021

mSphere

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Lsr2 is a nucleoid-associated protein (NAP) that has been found strictly in actinobacteria, including mycobacteria. It is a functional homolog of histone-like nucleoid-structuring protein (H-NS); it acts as a DNA-bridging protein that plays a role in chromosomal organization and transcriptional regulation. To date, the studies on Lsr2 have focused mainly on Mycobacterium tuberculosis. In this study, we analyze the role of Lsr2 as a transcription factor in Mycobacterium smegmatis, a saprophytic bacterium whose natural habitat (soil and water) substantially differs from those of the obligatory mycobacterial pathogens. Our chromatin immunoprecipitation-sequencing (ChIP-seq) data revealed that Lsr2 binds preferentially to AT-rich regions of the M. smegmatis chromosome. We found that Lsr2 acts mainly as a repressor, controlling gene expression either directly by binding promoter regions or indirectly through DNA loop formation and DNA coating. One of the Lsr2-repressed genes encodes polyketide synthase (MSMEG_4727), which is involved in the synthesis of lipooligosaccharides (LOSs). An M. smegmatis strain deprived of Lsr2 produces more LOSs, which is mirrored by changes in the smoothness of cells and their susceptibilities to antibiotics. Unlike M. tuberculosis, M. smegmatis additionally encodes a paralogue of Lsr2, MSMEG_1060, which is a novel member of the mycobacterial NAP family. The Lsr2 and MSMEG_1060 proteins exhibit different DNA binding specificities and chromosomal localizations. Our results suggest that these proteins help M. smegmatis cells cope with stress conditions, including hypoxia and exposure to antibiotics. Thus, the present work provides novel insight into the role of Lsr2 paralogues in the ability of a saprophytic mycobacterial species to adjust to environmental changes. IMPORTANCE Nucleoid-associated proteins (NAPs) are the most abundant proteins involved in bacterial chromosome organization and global transcription regulation. The mycobacterial NAP family includes many diverse proteins; some are unique to actinobacteria, and many are crucial for survival under stress (e.g., HupB and Lsr2) and/or optimal growth conditions (e.g., mycobacterial integration host factor [mIHF]). Here, we present a comprehensive study concerning two functional homologues of mycobacterial H-NS: Lsr2 and its paralogue from M. smegmatis, MSMEG_1060. We found that Lsr2 plays a role in transcriptional regulation, mainly by repressing gene expression via DNA loop formation and/or DNA-coating mechanisms. Intriguingly, the number of Lsr2-mediated genes was found to increase under hypoxia. Compared to Lsr2, MSMEG_1060 exhibits a different DNA binding specificity and chromosomal localization. Since tuberculosis remains a serious worldwide health problem, studies on stress response-mediating agents, such as Lsr2, may contribute to the development of novel antituberculosis drugs.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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Lsr2 and Its Novel Paralogue Mediate the Adjustment of Mycobacterium smegmatis to Unfavorable Environmental Conditions

Kołodziej

Łebkowski

Płociński

et al. 2021

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“…Many other AT-rich genes, not of foreign origin, can also be recognized and regulated by xenogeneic silencers ( Navarre et al 2006 ; Castang et al 2008 ; Gordon et al 2010 ; Seid et al 2017 ). In addition, all known xenogeneic silencers also belong to the nucleoid-associated proteins (NAPs), which play important roles in chromosome organization and transcription regulation (for recent reviews, see Dame et al 2020 ; Hołówka and Zakrzewska-Czerwińska 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Xenogeneic Silencing and Bacterial Genome Evolution: Mechanisms for DNA Recognition Imply Multifaceted Roles of Xenogeneic Silencers

Duan

Ding

Navarre

et al. 2021

Molecular Biology and Evolution

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Horizontal gene transfer (HGT) is a major driving force for bacterial evolution. To avoid the deleterious effects due to the unregulated expression of newly-acquired foreign genes, bacteria have evolved specific proteins named xenogeneic silencers to recognize foreign DNA sequences and suppress their transcription. As there is considerable diversity in genomic base compositions among bacteria, how xenogeneic silencers distinguish self- from non-self DNA in different bacteria remains poorly understood. This review summarizes the progress in studying the DNA binding preferences and the underlying molecular mechanisms of known xenogeneic silencer families, represented by H-NS of Escherichia coli, Lsr2 of Mycobacterium, MvaT of Pseudomonas, and Rok of Bacillus. Comparative analyses of the published data indicate that the differences in DNA recognition mechanisms enable these xenogeneic silencers to have clear characteristics in DNA sequence preferences, which are further correlated with different host genomic features. These correlations provide insights into the mechanisms of how these xenogeneic silencers selectively target foreign DNA in different genomic backgrounds. Furthermore, it is revealed that the genomic AT contents of bacterial species with the same xenogeneic silencer family proteins are distributed in a limited range, and are generally lower than those species without any known xenogeneic silencers in the same phylum/class/genus, indicating that xenogeneic silencers have multifaceted roles on bacterial genome evolution. In addition to regulating horizontal gene transfer, xenogeneic silencers also act as a selective force against the GC to AT mutational bias found in bacterial genomes and help the host genomic AT contents maintained at relatively low levels.

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“…Prokaryotes have a similar DNA condensation mechanism and utilize nucleoid-associated proteins (NAPs) to condense their DNA. NAPs are small, basic proteins that condense the bacterial chromosome into microdomains and work as transcription regulators (10). Due to their functional similarity to eukaryotic histones, NAPs were known initially as histone-like proteins.…”

Section: Nucleoid Associated Proteinsmentioning

confidence: 99%

Structural Elucidation of an HU-Junction Complex

Khun¹

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Mariam, and Kaileen. From dressing up as the Holliday junction for Halloween to hiding pipettes and having scavenger hunts, I am so blessed to have found a family away from home. I also am grateful to Tithi, Katie, Swastik, and Dr. Heidi Erlandsen for their advice and help. A special shoutout to Sudipta and Zane who have become my older brothers and the Mukerji class of 2016-2018 for training me and answering all of my questions. I hope this pandemic ends soon so that we can go to Salsas 3 again! I also owe a lot of gratitude to my family and friends. Thank you for always listening to me and providing me with support and motivation. I would like to thank iii my partner, Khang, for all of his love and endless support. Finally, I would like to thank the MBB department, the GSA, and Barb and Cheryl.

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Nucleoid Associated Proteins: The Small Organizers That Help to Cope With Stress

Cited by 84 publications

References 75 publications

Lsr2 and Its Novel Paralogue Mediate the Adjustment of Mycobacterium smegmatis to Unfavorable Environmental Conditions

Lsr2 and Its Novel Paralogue Mediate the Adjustment of Mycobacterium smegmatis to Unfavorable Environmental Conditions

Xenogeneic Silencing and Bacterial Genome Evolution: Mechanisms for DNA Recognition Imply Multifaceted Roles of Xenogeneic Silencers

Structural Elucidation of an HU-Junction Complex

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