The L egionella pneumophila kai operon is implicated in stress response and confers fitness in competitive environments

Loza‐Correa, Maria; Sahr, Tobias; Rolando, Monica; Daniels, Craig; Petit, Pierre; Skarina, Tania; Gomez Valero, Laura; Dervins‐Ravault, Delphine; Honoré, Nadine; Savchenko, Aleksey; Buchrieser, Carmen

doi:10.1111/1462-2920.12223

Cited by 34Circadian rhythm and melatoninBacterial Genetics and BiotechnologyLegionella and Acanthamoeba research

The L egionella pneumophila kai operon is implicated in stress response and confers fitness in competitive environments

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Loza‐Correa, Maria, Sahr, Tobias, Rolando, Monica, Daniels, Craig, Petit, Pierre, Skarina, Tania, Gomez Valero, Laura, Dervins‐Ravault, Delphine +3 more·2014·Environmental Microbiology

DOI 10.1111/1462-2920.12223PMC PMC4113418

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Abstract

Summary: L egionella pneumophila uses aquatic protozoa as replication niche and protection from harsh environments. Although L . pneumophila is not known to have a circadian clock, it encodes homologues of the KaiBC proteins of C yanobacteria that regulate circadian gene expression. We show that L . pneumophila kaiB , kaiC and the downstream gene lpp1114 , are transcribed as a unit under the control of the stress sigma factor RpoS . KaiC and KaiB of L . pneumophila do not interact as evidenced by yeast and bacterial two‐hybrid analyses. Fusion of the C ‐terminal residues of cyanobacterial KaiB to L egionella KaiB restores their interaction. In contrast, KaiC of L . pneumophila conserved autophosphorylation activity, but KaiB does not trigger the dephosphorylation of KaiC like in C yanobacteria . The crystal structure of L . pneumophila KaiB suggests that it is an oxidoreductase‐like protein with a typical thioredoxin fold. Indeed, mutant analyses revealed that the kai operon‐encoded proteins increase fitness of L . pneumophila in competitive environments, and confer higher resistance to oxidative and sodium stress. The phylogenetic analysis indicates that L . pneumophila KaiBC resemble S ynechosystis KaiC2B2 and not circadian KaiB1C1 . Thus, the L . pneumophila K ai proteins do not encode a circadian clock, but enhance stress resistance and adaption to changes in the environments.

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A KaiB variant from Legionella pneumophila previously crystallized in the FS state was predicted with high confidence for the FS state.
“By contrast, a KaiB variant from Legionella pneumophila that has previously been crystallized in the FS state37 was predicted with high confidence for the FS state.”
From Predicting multiple conformations via sequence clustering and AlphaFold2 (2024) · cites this paper as [37]

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Doublet, P., Vincent, C., Grangeasse, C., Cozzone, A. J., & Duclos, B. (1999) · FEBS Letters · doi:10.1016/s0014-5793(99)00111-8 · Cited by 44 · see citing works
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Aquaporin AqpZ Is Involved in Cell Volume Regulation and Sensitivity to Osmotic Stress in Synechocystis sp. Strain PCC 6803
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Photocycle of the LOV ‐ STAS Protein from the Pathogen Listeria monocytogenes.
Chan, R. H., Lewis, J. W., & Bogomolni, R. A. (2012) · Photochemistry and Photobiology · doi:10.1111/php.12004 · Cited by 26 · see citing works
Blue Flickers of Hope: Secondary Structure, Dynamics, and Putative Dimerization Interface of the Blue-Light Receptor YtvA from Bacillus subtilis
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Draft Genome Sequences of Two Legionella dumoffii Strains, TEX-KL and NY-23
Qin, T., Cui, Y., Cen, Z., Liang, T., Ren, H., Yang, X., Zhao, X., Liu, Z., Xu, L., Li, D., et al. (2012) · Journal of Bacteriology · doi:10.1128/jb.06352-11 · Cited by 15 · see citing works
The Circadian Clock-Associated Small GTPase LIGHT INSENSITIVE PERIOD1 Suppresses Light-Controlled Endoreplication and Affects Tolerance to Salt Stress in Arabidopsis
Terecskei, K., Tóth, R., Gyula, P., Kevei, É., Bindics, J., Coupland, G., Nagy, F., & Kozma‐Bognár, L. (2012) · PLANT PHYSIOLOGY · doi:10.1104/pp.112.203356 · Cited by 12 · see citing works

Flagged first, then by citations

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Predicting multiple conformations via sequence clustering and AlphaFold2
Wayment-Steele, H. K., Ojoawo, A., Otten, R., Apitz, J. M., Pitsawong, W., Hömberger, M., Ovchinnikov, S., Colwell, L., & Kern, D. (2024) · Nature · doi:10.1038/s41586-023-06832-9 · Cited by 545 · see citing works
Circadian Rhythms in Cyanobacteria
Cohen, S., & Golden, S. S. (2015) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00036-15 · Cited by 290 · see citing works
A protein fold switch joins the circadian oscillator to clock output in cyanobacteria
Chang, Y.-G., Cohen, S. E., Phong, C., Myers, W. K., Kim, Y.-I., Tseng, R., Lin, J., Zhang, L., Boyd, J. S., Lee, Y., et al. (2015) · Science · doi:10.1126/science.1260031 · Cited by 212 · see citing works
Minimal tool set for a prokaryotic circadian clock
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Controlling the Cyanobacterial Clock by Synthetically Rewiring Metabolism
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Proteomics of intracellular Salmonella enterica reveals roles of Salmonella pathogenicity island 2 in metabolism and antioxidant defense
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Damped circadian oscillation in the absence of KaiA in Synechococcus
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Giving Time Purpose: The Synechococcus elongatus Clock in a Broader Network Context
Shultzaberger, R. K., Boyd, J. S., Diamond, S., Greenspan, R. J., & Golden, S. S. (2015) · Annual Review of Genetics · doi:10.1146/annurev-genet-111212-133227 · Cited by 34 · see citing works
Light-dependent expression of four cryptic archaeal circadian gene homologs
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Proposed Role for KaiC-Like ATPases as Major Signal Transduction Hubs in Archaea
Makarova, K. S., Galperin, M. Y., & Koonin, E. V. (2017) · mBio · doi:10.1128/mbio.01959-17 · Cited by 26 · see citing works
A high‐throughput predictive method for sequence‐similar fold switchers
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Circadian rhythms in infectious diseases and symbiosis
Rijo‐Ferreira, F., & Takahashi, J. S. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2021.09.004 · Cited by 23 · see citing works
Two KaiABC systems control circadian oscillations in one cyanobacterium
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The conformational landscape of fold-switcher KaiB is tuned to the circadian rhythm timescale
Wayment-Steele, H. K., Otten, R., Pitsawong, W., Ojoawo, A. M., Glaser, A., Calderone, L. A., & Kern, D. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2412293121 · Cited by 19 · see citing works
KaiC family proteins integratively control temperature‐dependent UV resistance in Methylobacterium extorquens AM1
Iguchi, H., Yoshida, Y., Fujisawa, K., Taga, H., Yurimoto, H., Oyama, T., & Sakai, Y. (2018) · Environmental Microbiology Reports · doi:10.1111/1758-2229.12662 · Cited by 18 · see citing works
Synechocystis KaiC3 Displays Temperature- and KaiB-Dependent ATPase Activity and Is Important for Growth in Darkness
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Temperature-dependent fold-switching mechanism of the circadian clock protein KaiB
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Circadian Rhythm Modulation of Microbes During Health and Infection
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Prokaryotic Circadian Systems: Cyanobacteria and Beyond
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Autophosphorylation of the KaiC‐like protein ArlH inhibits oligomerization and interaction with ArlI, the motor ATPase of the archaellum
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KidA, a multi-PAS domain protein, tunes the period of the cyanobacterial circadian oscillator
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Does Sequence Clustering Confound AlphaFold2?
(2025) · doi:10.1016/j.jmb.2025.169376 · Cited by 8 · see citing works
Single molecules can operate as primitive biological sensors, switches and oscillators
Hernansaiz-Ballesteros, R. D., Cardelli, L., & Csikász‐Nagy, A. (2018) · BMC Systems Biology · doi:10.1186/s12918-018-0596-4 · Cited by 8 · see citing works
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Minimal Tool Set for a Prokaryotic Circadian ClockPreprint
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Structural Analysis of a Metamorphic Protein using AlphaFold2Preprint
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KaiC-like ATPases as Signal Transduction Hubs in Archaea
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Two circadian oscillators in one cyanobacteriumPreprint
Köbler, C., Schmelling, N. M., Pawlowski, A., Spät, P., Scheurer, N. M., Sebastian, K. N., Berwanger, L. L., Maček, B., Wiegard, A., Axmann, I. M. I., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.07.20.453058 · Cited by 2 · see citing works
The elusive rhythms of bacterial life
Kay, H., & Jabbur, M. L. (2026) · FEBS Letters · doi:10.1002/1873-3468.70287

The role of the kai operon genes in Legionella pneumophila
Correa, M. L. (2013) · theses.fr (ABES)
Rôle de l’opéron kai chez Legionella pneumophila
Correa, M. L. (2013) · OpenGrey (Institut de l'Information Scientifique et Technique)
Legionella pneumophila OxyR Is a Redundant Transcriptional Regulator That Contributes to Expression Control of the Two-Component CpxRA System
Tanner, J. R., Patel, P. G., Hellinga, J. R., Donald, L. J., Jimenez, C., LeBlanc, J. J., & Brassinga, A. K. C. (2016) · Journal of Bacteriology · doi:10.1128/jb.00690-16 · Cited by 12 · see citing works
The Legionella pneumophila rpoS Gene Is Required for Growth within Acanthamoeba castellanii
Hales, L. M., & Shuman, H. A. (1999) · Journal of Bacteriology · doi:10.1128/jb.181.16.4879-4889.1999 · Cited by 185 · see citing works
Circadian Clock Proteins in Prokaryotes: Hidden Rhythms?
Loza‐Correa, M., Gómez-Valero, L., & Buchrieser, C. (2010) · Frontiers in Microbiology · doi:10.3389/fmicb.2010.00130 · Cited by 46 · see citing works
Self-citation

Authors: Loza‐Correa, M., Sahr, T., Rolando, M., Daniels, C., Petit, P., Skarina, T., Gomez Valero, L., Dervins‐Ravault, D., Honoré, N., Savchenko, A., & Buchrieser, C.
Affiliations: Centre National de la Recherche Scientifique (FR)
University of Toronto (CA)
Institut Pasteur Biologie des Bactéries Intracellulaires Paris France
Institut Pasteur (FR)
Corresponding author: Buchrieser, Carmen
ORCID: Rolando, Monica
Buchrieser, Carmen
Venue: Environmental Microbiology
Publisher: Wiley
Published: 2013-08-19
Volume: 16
Issue: 2
Pages: 359-381
ISSN: 1462-2912 (ISSN-L)
1462-2920
DOI: 10.1111/1462-2920.12223
PMC: PMC4113418
OpenAlex: W1596776796
Cited by: 34
References: 90
Citations by year: 2026: 1 · 2025: 3 · 2024: 6 · 2023: 2 · 2022: 1 · 2021: 6 · 2020: 2 · 2019: 2 · 2018: 2 · 2017: 3 · 2016: 1 · 2015: 4 · 2014: 1
FWCI: 1.08
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: other-oa
onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Environmental Microbiology (publishedVersion, other-oa)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
HAL (submittedVersion, other-oa)
Funders: Agence Nationale de la Recherche (10-LABX-62-IBEID, ANR‐10‐LABX‐62‐IBEID, ANR-10, ANR-10-LABX-0062, ANR-10-LABX-62)
Fondation pour la Recherche Médicale (ANR-10-LABX-62-IBEID, DEQ20120323697)
Consejo Nacional de Ciencia y Tecnología
University of Toronto
Centre National de la Recherche Scientifique (10-LABX-62-IBEID, ANR-10-LABX-62)
National Institutes of Health (GM094585, GM074942 and GM094585, GM074942)
National Institute of General Medical Sciences (U54GM094585, GM074942, GM094585, U54GM074942)
Topics: Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Legionella and Acanthamoeba research
Keywords: Legionella pneumophila, KaiB, KaiC, RpoS sigma factor, stress response, oxidative stress resistance, competitive fitness, circadian clock, thioredoxin fold, oxidative enzymes, phylogenetic analysis
MeSH terms: Adaptation, Physiological, Bacterial Proteins, Operon, Phosphorylation, Phylogeny, RNA, Bacterial, Stress, Physiological, Gene Expression Regulation, Bacterial, Legionella pneumophila, Protein Structure, Tertiary, Gene Expression Profiling, Acanthamoeba castellanii, Genetic Fitness, Circadian Rhythm Signaling Peptides and Proteins, Circadian Clocks

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The L egionella pneumophila kai operon is implicated in stress response and confers fitness in competitive environments

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