Cited by 318Redox biology and oxidative stressBacterial Genetics and BiotechnologyMetal-Catalyzed Oxygenation Mechanisms

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When anaerobes encounter oxygen: mechanisms of oxygen toxicity, tolerance and defence

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Lu, Zheng, Imlay, James A.·2021·Nature Reviews Microbiology

DOI 10.1038/s41579-021-00583-yPMC PMC9191689

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Abstract

The defining trait of obligate anaerobes is that oxygen blocks their growth, yet the underlying mechanisms are unclear. A popular hypothesis was that these microorganisms failed to evolve defences to protect themselves from reactive oxygen species (ROS) such as superoxide and hydrogen peroxide, and that this failure is what prevents their expansion to oxic habitats. However, studies reveal that anaerobes actually wield most of the same defences that aerobes possess, and many of them have the capacity to tolerate substantial levels of oxygen. Therefore, to understand the structures and real-world dynamics of microbial communities, investigators have examined how anaerobes such as Bacteroides, Desulfovibrio, Pyrococcus and Clostridium spp. struggle and cope with oxygen. The hypoxic environments in which these organisms dwell - including the mammalian gut, sulfur vents and deep sediments - experience episodic oxygenation. In this Review, we explore the molecular mechanisms by which oxygen impairs anaerobes and the degree to which bacteria protect their metabolic pathways from it. The emergent view of anaerobiosis is that optimal strategies of anaerobic metabolism depend upon radical chemistry and low-potential metal centres. Such catalytic sites are intrinsically vulnerable to direct poisoning by molecular oxygen and ROS. Observations suggest that anaerobes have evolved tactics that either minimize the extent to which oxygen disrupts their metabolism or restore function shortly after the stress has dissipated.

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Hydroperoxide metabolism in mammalian organs.
Chance, B., Sies, H., & Boveris, A. (1979) · Physiological Reviews · doi:10.1152/physrev.1979.59.3.527 · Cited by 5,827
The rise of oxygen in Earth's early ocean and atmosphere
Lyons, T. W., Reinhard, C. T., & Planavsky, N. J. (2014) · Nature · doi:10.1038/nature13068 · Cited by 2,810
Bacterial iron homeostasis
Andrews, S. C., Robinson, A. K., & Rodríguez-Quiñones, F. (2003) · FEMS Microbiology Reviews · doi:10.1016/s0168-6445(03)00055-x · Cited by 2,702
Bacteroides : the Good, the Bad, and the Nitty-Gritty
Wexler, H. M. (2007) · Clinical Microbiology Reviews · doi:10.1128/cmr.00008-07 · Cited by 2,388
OXIDATIVE STRESS IN MARINE ENVIRONMENTS: Biochemistry and Physiological Ecology
Lesser, M. P. (2005) · Annual Review of Physiology · doi:10.1146/annurev.physiol.68.040104.110001 · Cited by 1,829
The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium
Imlay, J. A. (2013) · Nature Reviews Microbiology · doi:10.1038/nrmicro3032 · Cited by 1,749
Self-citation
Crosstalk between microbiota-derived short-chain fatty acids and intestinal epithelial HIF augments tissue barrier function
Kelly, C. J., Zheng, L., Campbell, E. L., Saeedi, B., Scholz, C. C., Bayless, A. J., Wilson, K. E., Glover, L. E., Kominsky, D. J., Magnuson, A., et al. (2015) · Cell Host & Microbe · doi:10.1016/j.chom.2015.03.005 · Cited by 1,716
Dating the rise of atmospheric oxygen
Bekker, A., Holland, H. D., Wang, P.-L., Rumble, D., Stein, H. J., Hannah, J. L., Coetzee, L. L., & Beukes, N. J. (2004) · Nature · doi:10.1038/nature02260 · Cited by 1,435
Gut inflammation provides a respiratory electron acceptor for Salmonella
Winter, S., Thiennimitr, P., Winter, M. G., Butler, B. P., Huseby, D. L., Crawford, R. W., Russell, J. M., Bevins, C. L., Adams, L. G., Tsolis, R. M., et al. (2010) · Nature · doi:10.1038/nature09415 · Cited by 1,271
Reactive oxygen species and mitochondria: A nexus of cellular homeostasis
Dunn, J. D., Álvarez, L., Zhang, X., & Soldati, T. (2015) · Redox Biology · doi:10.1016/j.redox.2015.09.005 · Cited by 1,233
The Generation of Superoxide Radical during the Autoxidation of Hemoglobin
Misra, H. P., & Fridovich, I. (1972) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)44679-6 · Cited by 1,173
Long-term ecological impacts of antibiotic administration on the human intestinal microbiota
Jernberg, C., Löfmark, S., Edlund, C., & Jansson, J. K. (2007) · The ISME Journal · doi:10.1038/ismej.2007.3 · Cited by 1,134
The physiology and habitat of the last universal common ancestor
Weiss, M. C., Sousa, F. L., Mrnjavac, N., Neukirchen, S., Roettger, M., Nelson-Sathi, S., & Martin, W. F. (2016) · Nature Microbiology · doi:10.1038/nmicrobiol.2016.116 · Cited by 1,049
An Enzyme-Based Theory of Obligate Anaerobiosis: The Physiological Function of Superoxide Dismutase
McCord, J. M., Keele, B. B., & Fridovich, I. (1971) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.68.5.1024 · Cited by 973
Hydrogen peroxide sensing, signaling and regulation of transcription factors
Marinho, H. S., Real, C., Cyrne, L., Soares, H., & Antunes, F. (2014) · Redox Biology · doi:10.1016/j.redox.2014.02.006 · Cited by 872
Biochemistry and Evolution of Anaerobic Energy Metabolism in Eukaryotes
Müller, M., Mentel, M., van Hellemond, J. J., Henze, K., Woehle, C., Gould, S. B., Yu, R.-Y., van der Giezen, M., Tielens, A. G. M., & Martin, W. F. (2012) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.05024-11 · Cited by 838
Comparison of fermentation reactions in different regions of the human colon
Macfarlane, G. T., Gibson, G. R., & Cummings, J. H. (1992) · Journal of Applied Bacteriology · doi:10.1111/j.1365-2672.1992.tb04882.x · Cited by 676
The inactivation of Fe-S cluster containing hydro-lyases by superoxide
Flint, D. H., Tuminello, J. F., & Emptage, M. H. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)41538-4 · Cited by 637
The evolution of cooperation within the gut microbiota
Rakoff-Nahoum, S., Foster, K. R., & Comstock, L. E. (2016) · Nature · doi:10.1038/nature17626 · Cited by 616
Superoxide and peroxynitrite inactivate aconitases, but nitric oxide does not.
Hausladen, A., & Fridovich, I. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)43893-8 · Cited by 585
The PerR transcription factor senses H2O2 by metal-catalysed histidine oxidation
Lee, J.-W., & Helmann, J. D. (2006) · Nature · doi:10.1038/nature04537 · Cited by 547
Superoxide sensitivity of the Escherichia coli aconitase.
Gardner, P. R., & Fridovich, I. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)55001-8 · Cited by 514
The cytochrome bd respiratory oxygen reductases
Borisov, V. B., Gennis, R. B., Hemp, J., & Verkhovsky, M. I. (2011) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2011.06.016 · Cited by 508
Physiologic hypoxia and oxygen homeostasis in the healthy intestine. A Review in the Theme: Cellular Responses to Hypoxia
Zheng, L., Kelly, C. J., & Colgan, S. P. (2015) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00191.2015 · Cited by 506
Dysbiosis in inflammatory bowel diseases: the oxygen hypothesis
Rigottier‐Gois, L. (2013) · The ISME Journal · doi:10.1038/ismej.2013.80 · Cited by 451
Evolution of Oxygenic Photosynthesis
Fischer, W. W., Hemp, J., & Johnson, J. E. (2016) · Annual Review of Earth and Planetary Sciences · doi:10.1146/annurev-earth-060313-054810 · Cited by 438
Oxidative stress and redox signaling mechanisms of inflammatory bowel disease: updated experimental and clinical evidence
Zhu, H., & Li, Y. R. (2012) · Experimental Biology and Medicine · doi:10.1258/ebm.2011.011358 · Cited by 432
The role of O2.− in the production of HO.: in vitro and in vivo
Liochev, S. I., & Fridovich, I. (1994) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(94)90239-9 · Cited by 423
Assay of metabolic superoxide production in Escherichia coli.
Imlay, J. A., & Fridovich, I. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(20)89596-9 · Cited by 420
Self-citation
Clostridia: the importance of their exceptional substrate and metabolite diversity for biofuel and biorefinery applications
Tracy, B. P., Jones, S. W., Fast, A. G., Indurthi, D. C., & Papoutsakis, E. T. (2011) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2011.10.008 · Cited by 408
Anaerobic Microbes: Oxygen Detoxification Without Superoxide Dismutase
Jenney, F. E., Verhagen, M. F. J. M., Cui, X., & Adams, M. W. W. (1999) · Science · doi:10.1126/science.286.5438.306 · Cited by 397
Role of oxygen gradients in shaping redox relationships between the human intestine and its microbiota
Espey, M. G. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2012.10.554 · Cited by 396
The free radical in pyruvate formate-lyase is located on glycine-734.
Wagner, A. F., Frey, M., Neugebauer, F. A., Schäfer, W. M., & Knappe, J. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.3.996 · Cited by 363
How oxygen attacks [FeFe] hydrogenases from photosynthetic organisms
Stripp, S. T., Goldet, G., Brandmayr, C., Sanganas, O., Vincent, K. A., Haumann, M., Armstrong, F. A., & Happe, T. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0905343106 · Cited by 361
Micromolar Intracellular Hydrogen Peroxide Disrupts Metabolism by Damaging Iron-Sulfur Enzymes
Jang, S., & Imlay, J. A. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m607646200 · Cited by 348
Self-citation
Inactivation-reactivation of aconitase in Escherichia coli. A sensitive measure of superoxide radical.
Gardner, P. R., & Fridovich, I. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)50343-x · Cited by 346
The gut anaerobe Faecalibacterium prausnitzii uses an extracellular electron shuttle to grow at oxic–anoxic interphases
Khan, M. T., Duncan, S. H., Stams, A. J. M., van Dijl, J. M., Flint, H. J., & Harmsen, H. J. M. (2012) · The ISME Journal · doi:10.1038/ismej.2012.5 · Cited by 343
Desulfovibrio Bacterial Species Are Increased in Ulcerative Colitis
Rowan, F., Docherty, N. G., Murphy, M., Murphy, B., Coffey, J. C., & O‘Connell, P. R. (2010) · Diseases of the Colon & Rectum · doi:10.1007/dcr.0b013e3181f1e620 · Cited by 333
Where in the world do bacteria experience oxidative stress?
Imlay, J. A. (2018) · Environmental Microbiology · doi:10.1111/1462-2920.14445 · Cited by 329
Self-citation
The strict anaerobe Bacteroides fragilis grows in and benefits from nanomolar concentrations of oxygen
Baughn, A. D., & Malamy, M. H. (2004) · Nature · doi:10.1038/nature02285 · Cited by 325
Suspect terranes and accretionary history of the Appalachian orogen
Williams, H., & Hatcher, R. D. (1982) · Geology · doi:10.1130/0091-7613(1982)10 · Cited by 325
Oxygen as a driver of gut dysbiosis
Rivera-Chávez, F., Lopez, C. A., & Bäumler, A. J. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.09.022 · Cited by 321
Escherichia coli Habitats, Cell Types, and Molecular Mechanisms of Gene Control
Savageau, M. A. (1983) · The American Naturalist · doi:10.1086/284168 · Cited by 315
The contribution of sulphate reducing bacteria and 5-aminosalicylic acid to faecal sulphide in patients with ulcerative colitis
Pitcher, M. (2000) · Gut · doi:10.1136/gut.46.1.64 · Cited by 297
Iron–sulfur proteins with nonredox functions
Flint, D. H., & Allen, R. M. (1996) · Chemical Reviews · doi:10.1021/cr950041r · Cited by 280
Microbes vs. chemistry in the origin of the anaerobic gut lumen
Friedman, E. S., Bittinger, K. L., Esipova, T. V., Hou, L., Chau, L., Jiang, J., Mesaros, C., Lund, P. J., Liang, X., FitzGerald, G. A., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1718635115 · Cited by 272
Factors Contributing to Hydrogen Peroxide Resistance in Streptococcus pneumoniae Include Pyruvate Oxidase (SpxB) and Avoidance of the Toxic Effects of the Fenton Reaction
Pericone, C. D., Park, S., Imlay, J. A., & Weiser, J. N. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.23.6815-6825.2003 · Cited by 270
Self-citation
Superoxide sensitivity of the Escherichia coli 6-phosphogluconate dehydratase
Gardner, P. R., & Fridovich, I. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)52319-x · Cited by 264
Pyruvate oxidase, as a determinant of virulence in Streptococcus pneumoniae
Spellerberg, B., Cundell, D. R., Sandros, J., Pearce, B. J., Idänpään‐Heikkilä, I., Rosenow, C., & Masure, H. R. (1996) · Molecular Microbiology · doi:10.1046/j.1365-2958.1996.425954.x · Cited by 264
Competition and coexistence of sulfate-reducing and methanogenic populations in anaerobic biofilms
Raskin, L. M., Rittmann, B. E., & Stahl, D. A. (1996) · Applied and Environmental Microbiology · doi:10.1128/aem.62.10.3847-3857.1996 · Cited by 261
Pyruvate Ferredoxin Oxidoreductase and Its Radical Intermediate
Ragsdale, S. W. (2003) · Chemical Reviews · doi:10.1021/cr020423e · Cited by 259
alpha, beta-Dihydroxyisovalerate dehydratase. A superoxide-sensitive enzyme.
Kuo, C. F., Mashino, T., & Fridovich, I. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)61255-4 · Cited by 247
Shallow breathing: bacterial life at low O2
Morris, R. L., & Schmidt, T. M. (2013) · Nature Reviews Microbiology · doi:10.1038/nrmicro2970 · Cited by 240
REACTIVE OXYGEN INTERMEDIATES IN BIOCHEMISTRY
Naqui, A., Chance, B., & Cadenas, E. (1986) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.55.070186.001033 · Cited by 234
Antibiotic Treatment Affects Intestinal Permeability and Gut Microbial Composition in Wistar Rats Dependent on Antibiotic Class
Tulstrup, M. V.-L., Christensen, E. G., Carvalho, V., Linninge, C., Ahrné, S., Højberg, O., Licht, T. R., & Bahl, M. I. (2015) · PLoS ONE · doi:10.1371/journal.pone.0144854 · Cited by 232
Geobacter sulfurreducens Can Grow with Oxygen as a Terminal Electron Acceptor
Lin, W. C., Coppi, M. V., & Lovley, D. R. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.4.2525-2528.2004 · Cited by 222
Methyl (Alkyl)-Coenzyme M Reductases: Nickel F-430-Containing Enzymes Involved in Anaerobic Methane Formation and in Anaerobic Oxidation of Methane or of Short Chain Alkanes
Thauer, R. K. (2019) · Biochemistry · doi:10.1021/acs.biochem.9b00164 · Cited by 214
The Generation of Superoxide Radical during the Autoxidation of Ferredoxins
Misra, H. P., & Fridovich, I. (1971) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)45929-2 · Cited by 214
Hydrogen peroxide inactivates the Escherichia coli Isc iron‐sulphur assembly system, and OxyR induces the Suf system to compensate
Jang, S., & Imlay, J. A. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2010.07418.x · Cited by 213
Self-citation
Two biochemically distinct classes of fumarase in Escherichia coli
Woods, S. A., Schwartzbach, S. D., & Guest, J. R. (1988) · Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology · doi:10.1016/0167-4838(88)90050-7 · Cited by 206
The role of biology in planetary evolution: cyanobacterial primary production in low‐oxygen Proterozoic oceans
Hamilton, T. L., Bryant, D. A., & Macalady, J. L. (2015) · Environmental Microbiology · doi:10.1111/1462-2920.13118 · Cited by 197
Two sources of endogenous hydrogen peroxide in Escherichia coli
Korshunov, S., & Imlay, J. A. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2010.07059.x · Cited by 184
Self-citation
Respiratory Protection of Nitrogenase Activity in Azotobacter vinelandii—Roles of the Terminal Oxidases
Poole, R. K., & Hill, S. (1997) · Bioscience Reports · doi:10.1023/a:1027336712748 · Cited by 171
Evolution of Nitrate Reductase: Molecular and Structural Variations on a Common Function
Stolz, J. F., & Basu, P. (2002) · ChemBioChem · doi:10.1002/1439-7633(20020301)3:2/3 · Cited by 171
[FeFe]-Hydrogenase Oxygen Inactivation Is Initiated at the H Cluster 2Fe Subcluster
Swanson, K. D., Ratzloff, M. W., Mulder, D. W., Artz, J. H., Ghose, S., Hoffman, A., White, S. N., Zadvornyy, O. A., Broderick, J. B., Bothner, B. B., et al. (2015) · Journal of the American Chemical Society · doi:10.1021/ja510169s · Cited by 156
Oxygen tolerance of fresh clinical anaerobic bacteria
Tally, F. P., Stewart, P., Sutter, V. L., & Rosenblatt, J. E. (1975) · Journal of Clinical Microbiology · doi:10.1128/jcm.1.2.161-164.1975 · Cited by 154
Mechanism of O2 diffusion and reduction in FeFe hydrogenases
Kubas, A., Orain, C., Sancho, D. D., Saujet, L., Sensi, M., Gauquelin, C., Meynial‐Salles, I., Soucaille, P., Bottin, H., Baffert, C., et al. (2016) · Nature Chemistry · doi:10.1038/nchem.2592 · Cited by 152
Rubredoxin Oxidase, a New Flavo-Hemo-Protein, Is the Site of Oxygen Reduction to Water by the "Strict Anaerobe" Desulfovibrio gigas
Chen, L., Liu, M., LeGall, J., Fareleira, P., Santos, H., & Xavier, A. V. (1993) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1993.1595 · Cited by 145
A glycyl radical solution: oxygen‐dependent interconversion of pyruvate formate‐lyase
Sawers, R. G., & Watson, G. M. F. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00941.x · Cited by 137
A Flavodiiron Protein and High Molecular Weight Rubredoxin from Moorella thermoacetica with Nitric Oxide Reductase Activity
Silaghi-Dumitrescu, R. L., Coulter, E. D., Das, A., Ljungdahl, L. G., Jameson, G. N. L., Huynh, B. H., & Kurtz, D. M. J. (2003) · Biochemistry · doi:10.1021/bi027253k · Cited by 126
Escherichia coli cytochrome c peroxidase is a respiratory oxidase that enables the use of hydrogen peroxide as a terminal electron acceptor
Khademian, M., & Imlay, J. A. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1701587114 · Cited by 126
Self-citation
Oxygen-dependent growth of the obligate anaerobe Desulfovibrio vulgaris Hildenborough
Johnson, M. S., Zhulin, I. B., Gapuzan, M. E., & Taylor, B. L. (1997) · Journal of Bacteriology · doi:10.1128/jb.179.17.5598-5601.1997 · Cited by 124
Inactivation of Dehydratase [4Fe-4S] Clusters and Disruption of Iron Homeostasis upon Cell Exposure to Peroxynitrite
Keyer, K., & Imlay, J. A. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.44.27652 · Cited by 119
Self-citation
The Bacteroides fragilis transcriptome response to oxygen and H2O2: the role of OxyR and its effect on survival and virulence
Sund, C. J., Rocha, E. R., Tzinabos, A. O., Wells, W. G., Gee, J. M., Reott, M. A., O’Rourke, D. P., & Smith, C. J. (2007) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.06031.x · Cited by 119
Cell-Wide Responses to Low-Oxygen Exposure inDesulfovibrio vulgarisHildenborough
Mukhopadhyay, A., Redding, A. M., Joachimiak, M. P., Arkin, A. P., Borglin, S. E., Dehal, P., Chakraborty, R., Geller, J. T., Hazen, T. C., He, Q., et al. (2007) · Journal of Bacteriology · doi:10.1128/jb.00368-07 · Cited by 119
PerR acts as a switch for oxygen tolerance in the strict anaerobe Clostridium acetobutylicum
Hillmann, F., Fischer, R., Saint‐Prix, F., Girbal, L., & Bahl, H. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06192.x · Cited by 114
How does oxygen inhibit central metabolism in the obligate anaerobe Bacteroides thetaiotaomicron
Pan, N., & Imlay, J. A. (2001) · Molecular Microbiology · doi:10.1046/j.1365-2958.2001.02343.x · Cited by 113
Self-citation
Hydrogen Peroxide Production in Streptococcus pyogenes : Involvement of Lactate Oxidase and Coupling with Aerobic Utilization of Lactate
Seki, M., Iida, K., Saito, M., Nakayama, H., & Yoshida, S. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.7.2046-2051.2004 · Cited by 107
Superoxide poisons mononuclear iron enzymes by causing mismetallation
Gu, M., & Imlay, J. A. (2013) · Molecular Microbiology · doi:10.1111/mmi.12263 · Cited by 105
Self-citation
Dehydration of (R)-2-hydroxyacyl-CoA to enoyl-CoA in the fermentation of α-amino acids by anaerobic bacteria
Kim, J., Hetzel, M., Boiangiu, C. D., & Buckel, W. (2004) · FEMS Microbiology Reviews · doi:10.1016/j.femsre.2004.03.001 · Cited by 103
Function of Oxygen Resistance Proteins in the Anaerobic, Sulfate-Reducing Bacterium Desulfovibrio vulgaris Hildenborough
Fournier, M. L., Zhang, Y., Wildschut, J. D., Dolla, A. R., Voordouw, J. K., Schriemer, D. C., & Voordouw, G. (2002) · Journal of Bacteriology · doi:10.1128/jb.185.1.71-79.2003 · Cited by 103
Adaptive Responses to Oxygen Stress in Obligatory Anaerobes Clostridium acetobutylicum and Clostridium aminovalericum
Kawasaki, S., Watamura, Y., Ono, M., Watanabe, T., Takeda, K., & Niimura, Y. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.12.8442-8450.2005 · Cited by 100
Pyruvate formate-lyase mechanism involving the protein-based glycyl radical
Knappe, J., Elbert, S., Frey, M., & Wagner, A. (1993) · Biochemical Society Transactions · doi:10.1042/bst0210731 · Cited by 98
Cytochrome bd Oxidase, Oxidative Stress, and Dioxygen Tolerance of the Strictly Anaerobic Bacterium Moorella thermoacetica
Das, A., Silaghi-Dumitrescu, R. L., Ljungdahl, L. G., & Kurtz, D. M. J. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.6.2020-2029.2005 · Cited by 97
Ferredoxins of the third kind
Meyer, J. (2001) · FEBS Letters · doi:10.1016/s0014-5793(01)03049-6 · Cited by 92
An anaerobic bacterium, B acteroides thetaiotaomicron, uses a consortium of enzymes to scavenge hydrogen peroxide
Mishra, S., & Imlay, J. A. (2013) · Molecular Microbiology · doi:10.1111/mmi.12438 · Cited by 91
Self-citation
The Redox-Sensitive Transcriptional Activator OxyR Regulates the Peroxide Response Regulon in the Obligate Anaerobe Bacteroides fragilis
Rocha, E. R., Owens, G. K., & Smith, C. J. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.18.5059-5069.2000 · Cited by 86
The Peritoneal Environment During Infection
Sawyer, R. G., Spengler, M. D., Adams, R. B., & Pruett, T. L. (1991) · Annals of Surgery · doi:10.1097/00000658-199103000-00013 · Cited by 81
Dps biomineralizing proteins: multifunctional architects of nature
Zeth, K. (2012) · Biochemical Journal · doi:10.1042/bj20120514 · Cited by 80
Improved measurements of scant hydrogen peroxide enable experiments that define its threshold of toxicity for Escherichia coli
Li, X., & Imlay, J. A. (2018) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.03.025 · Cited by 80
Self-citation
Evolution and diversification of Group 1 [NiFe] hydrogenases. Is there a phylogenetic marker for O2-tolerance?
Pandelia, M., Lubitz, W., & Nitschke, W. (2012) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2012.04.012 · Cited by 77
A Flavo-Diiron Protein from Desulfovibrio vulgaris with Oxidase and Nitric Oxide Reductase Activities. Evidence for an in Vivo Nitric Oxide Scavenging Function
Silaghi-Dumitrescu, R. L., Ng, K. Y., Viswanathan, R., & Kurtz, D. M. J. (2005) · Biochemistry · doi:10.1021/bi0477337 · Cited by 76
Dioxygen Inactivation of Pyruvate Formate-Lyase: EPR Evidence for the Formation of Protein-Based Sulfinyl and Peroxyl Radicals
Reddy, S. G., Wong, K. K., Parast, C. V., Peisach, J., Magliozzo, R. S., & Kozarich, J. W. (1998) · Biochemistry · doi:10.1021/bi972086n · Cited by 74
Oxygen permeability of thylakoid membranes: electron paramagnetic resonance spin labeling study
Ligeza, A., Tikhonov, A. N., Hyde, J. S., & Subczynski, W. K. (1998) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(98)00098-x · Cited by 72
Modulation of the Fumarases of Escherichia coli in Response to Oxidative Stress
Liochev, S. I., & Fridovich, I. (1993) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1993.1159 · Cited by 72
Discovery of superoxide reductase: an historical perspective
Nivière, V., & Fontecave, M. (2004) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-003-0519-7 · Cited by 72
Effect of ambient oxygen concentration on activities of enzymatic antioxidant defences and aerobic metabolism in the hydrothermal vent worm, Paralvinella grasslei
Marie, B., Génard, B., Rees, J., & Zal, F. (2006) · Marine Biology · doi:10.1007/s00227-006-0338-9 · Cited by 68
Rubredoxin:Oxygen Oxidoreductase Enhances Survival of Desulfovibrio vulgaris Hildenborough under Microaerophilic Conditions
Wildschut, J. D., Lang, R., Voordouw, J. K., & Voordouw, G. (2006) · Journal of Bacteriology · doi:10.1128/jb.00425-06 · Cited by 68
Intracellular Hydrogen Peroxide and Superoxide Poison 3-Deoxy-D-Arabinoheptulosonate 7-Phosphate Synthase, the First Committed Enzyme in the Aromatic Biosynthetic Pathway of Escherichia coli
Sobota, J. M., Gu, M., & Imlay, J. A. (2014) · Journal of Bacteriology · doi:10.1128/jb.01573-14 · Cited by 65
Self-citation
The Role of PerR in O2-Affected Gene Expression ofClostridium acetobutylicum
Hillmann, F., Döring, C., Riebe, O., Ehrenreich, A., Fischer, R., & Bahl, H. (2009) · Journal of Bacteriology · doi:10.1128/jb.00351-09 · Cited by 65
Mechanism of oxygen detoxification by the surprisingly oxygen-tolerant hyperthermophilic archaeon, Pyrococcus furiosus
Thorgersen, M. P., Stirrett, K. L., Scott, R. A., & Adams, M. W. W. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1208605109 · Cited by 62
BACTERIAL FERREDOXIN
Valentine, R. C. (1964) · Bacteriological Reviews · doi:10.1128/br.28.4.497-517.1964 · Cited by 59
Updates on the sporulation process in Clostridium species
Talukdar, P. K., Olguín-Araneda, V., Alnoman, M. M., Paredes‐Sabja, D., & Sarker, M. R. (2014) · Research in Microbiology · doi:10.1016/j.resmic.2014.12.001 · Cited by 57
Oxidative stress protection and the repair response to hydrogen peroxide in the hyperthermophilic archaeon Pyrococcus furiosus and in related species
Strand, K. R., Sun, C., Li, T., Jenney, F. E., Schut, G. J., & Adams, M. W. W. (2010) · Archives of Microbiology · doi:10.1007/s00203-010-0570-z · Cited by 54
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Lu, Z., Ramakrishnan, S., & Imlay, J. A. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1800120115 · Cited by 54
Self-citation
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Imlay, J. A., Ramakrishnan, S., & Rohaun, S. K. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.01.048 · Cited by 54
Self-citation
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Rocha, E. R., Herren, C. D., Smalley, D. J., & Smith, C. J. (2003) · Anaerobe · doi:10.1016/s1075-9964(03)00118-5 · Cited by 54
Oxygen Reductases in Alphaproteobacterial Genomes: Physiological Evolution From Low to High Oxygen Environments
Esposti, M. D., Mentel, M., Martin, W. F., & Sousa, F. L. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00499 · Cited by 50
The Escherichia coli yhjA gene, encoding a predicted cytochrome c peroxidase, is regulated by FNR and OxyR
Partridge, J. D., Poole, R. K., & Green, J. D. (2007) · Microbiology · doi:10.1099/mic.0.2006/004838-0 · Cited by 48
Metabolic response of Clostridium ljungdahlii to oxygen exposure
Whitham, J. M., Tirado-Acevedo, O., Chinn, M. S., Pawlak, J. J., & Grunden, A. M. (2015) · Applied and Environmental Microbiology · doi:10.1128/aem.02491-15 · Cited by 47
Initial Kinetic and Mechanistic Characterization of Escherichia coli Fumarase A
Flint, D. H. (1994) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1994.1269 · Cited by 47
Breathless in the Gut: Implications of Luminal O 2 for Microbial Pathogenicity
Kelly, C. J., & Colgan, S. P. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.03.014 · Cited by 46
Human colon function ex vivo: Dependence on oxygen and sensitivity to antibiotic
Schwerdtfeger, L., Nealon, N. J., Ryan, E. P., & Tobet, S. A. (2019) · PLoS ONE · doi:10.1371/journal.pone.0217170 · Cited by 45
Aerobic-Type Ribonucleotide Reductase in the Anaerobe Bacteroides fragilis
Smalley, D. J., Rocha, E. R., & Smith, C. J. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.4.895-903.2002 · Cited by 45
Ferritin-like family proteins in the anaerobe Bacteroides fragilis: when an oxygen storm is coming, take your iron to the shelter
Rocha, E. R., & Smith, C. J. (2013) · BioMetals · doi:10.1007/s10534-013-9650-2 · Cited by 43
Inactivation of Pyruvate Formate-Lyase by Dioxygen: Defining the Mechanistic Interplay of Glycine 734 and Cysteine 419 by Rapid Freeze-Quench EPR
Zhang, W., Wong, K. K., Magliozzo, R. S., & Kozarich, J. W. (2001) · Biochemistry · doi:10.1021/bi002589k · Cited by 43
Oxygen tolerance of human intestinal anaerobes
Rolfe, R. D., Hentges, D. J., Jt, B., & Campbell, B. J. (1977) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/30.11.1762 · Cited by 42
How to define obligatory anaerobiosis? An evolutionary view on the antioxidant response system and the early stages of the evolution of life on Earth
Ślesak, I., Kula-Maximenko, M., Ślesak, H., Miszalski, Z., & Strzałka, K. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.03.004 · Cited by 41
Disulfide Bond-Dependent Mechanism of Protection against Oxidative Stress in Pyruvate-Ferredoxin Oxidoreductase of Anaerobic Desulfovibrio Bacteria
Vita, N., Hatchikian, E. C., Nouailler, M., Dolla, A. R., & Pieulle, L. (2007) · Biochemistry · doi:10.1021/bi7014713 · Cited by 40
The Fumarate Reductase of Bacteroides thetaiotaomicron , unlike That of Escherichia coli , Is Configured so that It Does Not Generate Reactive Oxygen Species
Lu, Z., & Imlay, J. A. (2017) · mBio · doi:10.1128/mbio.01873-16 · Cited by 40
Self-citation
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Khademian, M., & Imlay, J. A. (2020) · Molecular Microbiology · doi:10.1111/mmi.14516 · Cited by 32
Self-citation
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Shibata, N., & Toraya, T. (2015) · The Journal of Biochemistry · doi:10.1093/jb/mvv078 · Cited by 31
A conserved motif liganding the [4Fe–4S] cluster in [4Fe–4S] fumarases prevents irreversible inactivation of the enzyme during hydrogen peroxide stress
Lu, Z., & Imlay, J. A. (2019) · Redox Biology · doi:10.1016/j.redox.2019.101296 · Cited by 31
Self-citation
Enzyme catalyzed radical dehydrations of hydroxy acids
Buckel, W., Zhang, J., Friedrich, P., Parthasarathy, A., Li, H., Djurdjević, I., Dobbek, H., & Martins, B. M. (2011) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2011.11.009 · Cited by 30
Bacterioferritin protects the anaerobe Desulfovibrio vulgaris Hildenborough against oxygen
Figueiredo, M. C. O., Lobo, S. A. L., Carita, J. N., Nobre, L. S., & Saraiva, L. M. (2012) · Anaerobe · doi:10.1016/j.anaerobe.2012.06.001 · Cited by 29
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Fourn, C. L., Brasseur, G., Brochier‐Armanet, C., Pieulle, L., Brioukhanov, A. L., Ollivier, B., & Dolla, A. R. (2011) · Environmental Microbiology · doi:10.1111/j.1462-2920.2011.02439.x · Cited by 29
Study of the Thiol/Disulfide Redox Systems of the Anaerobe Desulfovibrio vulgaris Points Out Pyruvate:Ferredoxin Oxidoreductase as a New Target for Thioredoxin 1
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Intraperitoneal oxygen and carbon dioxide tensions in experimental adhesion disease and peritonitis
Renvall, S., & Niinikoski, J. (1975) · The American Journal of Surgery · doi:10.1016/0002-9610(75)90387-6 · Cited by 28
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Authors: Lu, Z., & Imlay, J. A.
Affiliations: Shantou University (CN)
University of Illinois Urbana-Champaign (US)
Corresponding author: Lu, Zheng
Imlay, James A.
ORCID: Lu, Zheng
Imlay, James A.
Venue: Nature Reviews Microbiology
Publisher: Springer Science and Business Media LLC
Published: 2021-06-28
Volume: 19
Issue: 12
Pages: 774-785
ISSN: 1740-1526 (ISSN-L)
1740-1534
DOI: 10.1038/s41579-021-00583-y
PMC: PMC9191689
OpenAlex: W3174803191
Cited by: 318
References: 139
Citations by year: 2026: 68 · 2025: 86 · 2024: 67 · 2023: 51 · 2022: 41 · 2021: 5
FWCI: 4.30
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Nature Reviews Microbiology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of General Medical Sciences (R37GM049640, R01GM049640, R01GM141252)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Physical Sciences › Chemistry › Inorganic Chemistry › Metal-Catalyzed Oxygenation Mechanisms
Keywords: obligate anaerobes, oxygen toxicity, reactive oxygen species, antioxidant defense, superoxide, hydrogen peroxide, oxygen tolerance, Bacteroides, Desulfovibrio, Pyrococcus, Clostridium, low oxygen environment, anaerobic metabolism, microbial communities
MeSH terms: Anaerobiosis, Bacteria, Anaerobic, Bacteroides, Clostridium, Desulfovibrio, Hydrogen Peroxide, Oxygen, Superoxides, Reactive Oxygen Species, Pyrococcus

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When anaerobes encounter oxygen: mechanisms of oxygen toxicity, tolerance and defence

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