journal article Open Access Dec 15, 2020

Stress Response of Mesosutterella multiformis Mediated by Nitrate Reduction

Microorganisms Vol. 8 No. 12 pp. 2003 · MDPI AG
View at Publisher Save 10.3390/microorganisms8122003
Abstract
Bacterial stress responses are closely associated with the survival and colonization of anaerobes in the human gut. Mesosutterella multiformis JCM 32464T is a novel member of the family Sutterellaceae, an asaccharolytic bacterium. We previously demonstrated energy generation via heme biosynthesis, which is coupled with nitrate reductase. Here, physiological and morphological changes in M. multiformis induced by exposure to nitrate were investigated. The ability of M. multiformis to reduce nitrate was determined using a colorimetric assay. A unique morphology was observed during nitrate reduction under anaerobic conditions. The association between nitrate concentration and cell size or cellular fatty acid composition was evaluated. Nitrate-induced responses of M. multiformis were compared to those of related species. An increase in cellular filamentation and the ratio of saturated: unsaturated fatty acids was mediated specifically by nitrate. This indicates a decrease in cell fluidity and low leakage. Furthermore, a similar response was not observed in other related species cultured in the presence of nitrate. Hence, the nitrate-induced stress response in new anaerobes such as M. multiformis was demonstrated. The response could also be involved in the conservation of menaquinones and the maximization of nitrate reduction.
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References
38
[1]
Stress Physiology of Lactic Acid Bacteria

Konstantinos Papadimitriou, Angel Alegría, Peter A. Bron et al.

Microbiology and Molecular Biology Reviews 2016 10.1128/mmbr.00076-15
[2]
"Lactic acid bacteria stress response to preservation processes in the beverage and juice industry" Acta Biochim. Pol. (2017) 10.18388/abp.2017_1496
[3]
Hews "Maintaining integrity under stress: Envelope stress response regulation of pathogenesis in Gram-negative bacteria" Front. Cell. Infect. Microbiol. (2019) 10.3389/fcimb.2019.00313
[4]
Sakamoto "Mesosutterella multiformis gen. nov., sp. nov., a member of the family Sutterellaceae and Sutterella megalosphaeroides sp. nov., isolated from human faeces" Int. J. Syst. Evol. Microbiol. (2018) 10.1099/ijsem.0.003096
[5]
Williams "Application of novel PCR-based methods for detection, quantitation, and phylogenetic characterization of Sutterella species in intestinal biopsy samples from children with autism and gastrointestinal disturbances" mBio (2012) 10.1128/mbio.00261-11
[6]
Hiippala "Mucosal prevalence and interactions with the epithelium indicate commensalism of Sutterella spp." Front. Microbiol. (2016) 10.3389/fmicb.2016.01706
[7]
Chen "Parasutterella, in association with irritable bowel syndrome and intestinal chronic inflammation" J. Gastroenterol. Hepatol. (2018) 10.1111/jgh.14281
[8]
Ikeyama "Draft genome sequence of Mesosutterella multiformis JCM 32464T, a member of the family Sutterellaceae, isolated from human feces" Microbiol. Resour. Announc. (2019) 10.1128/mra.00478-19
[9]
Breckau "Heme biosynthesis is coupled to electron transport chains for energy generation" Proc. Natl. Acad. Sci. USA (2010) 10.1073/pnas.1000956107
[10]
Tiso, M., and Schechter, A.N. (2015). Nitrate reduction to nitrite, nitric oxide and ammonia by gut bacteria under physiological conditions. PLoS ONE, 10. 10.1371/journal.pone.0127490
[11]
Platzen "Role of flavohaemoprotein Hmp and nitrate reductases NarGHJI of Corynebacterium glutamicum for coping with nitrite and nitrosative stress" FEMS Microbiol. Lett. (2014) 10.1111/1574-6968.12318
[12]
Sakamoto "Faecalimonas umbilicata gen. nov., sp. nov., isolated from human faeces, and reclassification of Eubacterium contortum, Eubacterium fissicatena and Clostridium oroticum as Faecalicatena contorta gen. nov., comb. nov., Faecalicatena fissicatena comb. nov. and Faecalicatena orotica comb. nov" Int. J. Syst. Evol. Microbiol. (2017) 10.1099/ijsem.0.001790
[13]
Kuykendall "Fatty acids, antibiotic resistance, and deoxyribonucleic acid homology groups of Bradyrhizobium japonicum" Int. J. Syst. Bacteriol. (1988) 10.1099/00207713-38-4-358
[14]
Miller "Single derivatization method for routine analysis of bacterial whole-cell fatty acid methyl esters, including hydroxy acids" J. Clin. Microbiol. (1982) 10.1128/jcm.16.3.584-586.1982
[15]
KEGG: new perspectives on genomes, pathways, diseases and drugs

Minoru Kanehisa, Miho Furumichi, Mao Tanabe et al.

Nucleic Acids Research 2017 10.1093/nar/gkw1092
[16]
The RAST Server: Rapid Annotations using Subsystems Technology

Ramy K Aziz, Daniela Bartels, Aaron A Best et al.

BMC Genomics 10.1186/1471-2164-9-75
[17]
Tanizawa "DFAST: A flexible prokaryotic genome annotation pipeline for faster genome publication" Bioinformatics (2018) 10.1093/bioinformatics/btx713
[18]
Liu "The change of the state of cell membrane can enhance the synthesis of menaquinone in Escherichia coli" World J. Microbiol. Biotechnol. (2017) 10.1007/s11274-017-2222-9
[19]
Heinemann "The biochemistry of heme biosynthesis" Arch. Biochem. Biophys. (2008) 10.1016/j.abb.2008.02.015
[20]
Wexler "Sutterella wadsworthensis gen. nov., sp. nov., bile-resistant microaerophilic Campylobacter gracilis-like clinical isolates" Int. J. Syst. Bacteriol. (1996) 10.1099/00207713-46-1-252
[21]
Greetham "Sutterella stercoricanis sp. nov., isolated from canine faeces" Int. J. Syst. Evol. Microbiol. (2004) 10.1099/ijs.0.63098-0
[22]
Sakon "Sutterella parvirubra sp. nov. and Megamonas funiformis sp. nov., isolated from human faeces" Int. J. Syst. Evol. Microbiol. (2008) 10.1099/ijs.0.65456-0
[23]
Nagai "Parasutterella excrementihominis gen. nov., sp. nov., a member of the family Alcaligenaceae isolated from human faeces" Int. J. Syst. Evol. Microbiol. (2009) 10.1099/ijs.0.002519-0
[24]
Morotomi "Parasutterella secunda sp. nov., isolated from human faeces and proposal of Sutterellaceae fam. nov. in the order Burkholderiales" Int. J. Syst. Evol. Microbiol. (2011) 10.1099/ijs.0.023556-0
[25]
Macarisin "Salmonella enterica filamentation induced by pelargonic acid is a transient morphotype" Appl. Environ. Microbiol. (2019) 10.1128/aem.02191-18
[26]
Yoon, M.Y., Lee, K.M., Park, Y., and Yoon, S.S. (2011). Contribution of cell elongation to the biofilm formation of Pseudomonas aeruginosa during anaerobic respiration. PLoS ONE, 6. 10.1371/journal.pone.0016105
[27]
Nishimura "Gene expression profiling of Corynebacterium glutamicum during anaerobic nitrate respiration: Induction of the SOS response for cell survival" J. Bacteriol. (2011) 10.1128/jb.01453-10
[28]
Hoffmann "The anaerobic life of Bacillus subtilis: Cloning of the genes encoding the respiratory nitrate reductase system" FEMS Microbiol. Lett. (1995) 10.1111/j.1574-6968.1995.tb07780.x
[29]
Mukhopadhya, I., Hansen, R., Nicholl, C.E., Alhaidan, Y.A., Thomson, J.M., Berry, S.H., Pattinson, C., Stead, D.A., Russell, R.K., and El-Omar, E.M. (2011). A comprehensive evaluation of colonic mucosal isolates of Sutterella wadsworthensis from inflammatory bowel disease. PLoS ONE, 6. 10.1371/journal.pone.0027076
[30]
Szalontai "Membrane dynamics as seen by fourier transform infrared spectroscopy in a cyanobacterium, Synechocystis PCC 6803. The effects of lipid unsaturation and the protein-to-lipid ratio" Biochim. Biophys. Acta (2000) 10.1016/s0005-2736(00)00323-0
[31]
Sasarman "Role of menaquinone in nitrate respiration in Staphylococcus aureus" J. Bacteriol. (1974) 10.1128/jb.117.2.911-913.1974
[32]
Haddaji "Change in cell surface properties of Lactobacillus casei under heat shock treatment" FEMS Microbiol. Lett. (2015) 10.1093/femsle/fnv047
[33]
Gandhi "Effect of salt stress on morphology and membrane composition of Lactobacillus acidophilus, Lactobacillus casei, and Bifidobacterium bifidum, and their adhesion to human intestinal epithelial-like Caco-2 cells" J. Dairy Sci. (2016) 10.3168/jds.2015-10718
[34]
Archer "Evidence that ingested nitrate and nitrite are beneficial to health" J. Food Prot. (2002) 10.4315/0362-028x-65.5.872
[35]
Shaw "Formation of filaments and synthesis of macromolecules at temperatures below the minimum for growth of Escherichia coli" J. Bacteriol. (1968) 10.1128/jb.95.1.221-230.1968
[36]
Sajbidor "Effect of some environmental factors on the content and composition of microbial membrane lipids" Crit. Rev. Biotechnol. (1997) 10.3109/07388559709146608
[37]
Crompton, M.J., Dunstan, R.H., Macdonald, M.M., Gottfries, J., von Eiff, C., and Roberts, T.K. (2014). Small changes in environmental parameters lead to alterations in antibiotic resistance, cell morphology and membrane fatty acid composition in Staphylococcus lugdunensis. PLoS ONE, 9. 10.1371/journal.pone.0092296
[38]
Increased abundance of Sutterella spp. and Ruminococcus torques in feces of children with autism spectrum disorder

Lv Wang, Claus T Christophersen, Michael J Sorich et al.

Molecular Autism 2013 10.1186/2040-2392-4-42
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Published
Dec 15, 2020
Vol/Issue
8(12)
Pages
2003
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Funding
Japan Agency for Medical Research and Development Award: JP19gm6010007
Cite This Article
Nao Ikeyama, Moriya Ohkuma, Mitsuo Sakamoto (2020). Stress Response of Mesosutterella multiformis Mediated by Nitrate Reduction. Microorganisms, 8(12), 2003. https://doi.org/10.3390/microorganisms8122003
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