1887

Microbiology Society logo

Volume 158, Issue 8

Outer-membrane cytochrome-independent reduction of extracellular electron acceptors in Free

Abstract

Dissimilatory metal reduction under pH-neutral conditions is dependent on an extended respiratory chain to the cell surface. The final reduction is catalysed by outer-membrane cytochromes that transfer respiratory electrons either directly to mineral surfaces and metal ions bound in larger organic complexes such as Fe(III) citrate, or indirectly using endogenous or exogenous electron shuttles such as humic acids and flavins. Consequently, a deletion mutant devoid of outer-membrane cytochromes is unable to reduce Fe(III) citrate or manganese oxide minerals and reduces humic acids at lower rates. Surprisingly, the phenotype of this quintuple deletion mutant can be rescued by a suppressor mutation, which enables metal or humic acid reduction without any outer-membrane cytochrome. Furthermore, the type II secretion system, essential for metal reduction in wild-type , is not necessary for the suppressor strain. Using genome sequencing we identified two point mutations in key genes for metal reduction: and . These mutations are necessary and sufficient to account for the observed phenotype. This study is the first evidence for a catabolic, outer-membrane cytochrome-independent electron transport chain to ferric iron, manganese oxides and humic acid analogues operating in a mesophilic organism. Available bioinformatic data allow the hypothesis that outer-membrane cytochrome-independent electron transfer might resemble an evolutionary intermediate between ferrous iron-oxidizing and ferric iron-reducing micro-organisms.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
© Microbiology Society
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.058404-0
2012-08-01
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/8/2144.html?itemId=/content/journal/micro/10.1099/mic.0.058404-0&mimeType=html&fmt=ahah

References

  1. Aeschbacher M., Vergari D., Schwarzenbach R. P., Sander M. ( 2011). Electrochemical analysis of proton and electron transfer equilibria of the reducible moieties in humic acids. Environ Sci Technol 45:8385–8394 [View Article][PubMed]
     [Google Scholar]
  2. Bagos P. G., Liakopoulos T. D., Spyropoulos I. C., Hamodrakas S. J. ( 2004). A Hidden Markov Model method, capable of predicting and discriminating β-barrel outer membrane proteins. BMC Bioinformatics 5:29 [View Article][PubMed]
     [Google Scholar]
  3. Bayer M., Walter K., Simon H. ( 1996). Purification and partial characterisation of a reversible artificial mediator accepting NADH oxidoreductase from Clostridium thermoaceticum . Eur J Biochem 239:686–691 [View Article][PubMed]
     [Google Scholar]
  4. Belchik S. M., Kennedy D. W., Dohnalkova A. C., Wang Y., Sevinc P. C., Wu H., Lin Y., Lu H. P., Fredrickson J. K., Shi L. ( 2011). Extracellular reduction of hexavalent chromium by cytochromes MtrC and OmcA of Shewanella oneidensis MR-1. Appl Environ Microbiol 77:4035–4041 [View Article][PubMed]
     [Google Scholar]
  5. Beliaev A. S., Saffarini D. A. ( 1998). Shewanella putrefaciens mtrB encodes an outer membrane protein required for Fe(III) and Mn(IV) reduction. J Bacteriol 180:6292–6297[PubMed]
     [Google Scholar]
  6. Beliaev A. S., Saffarini D. A., McLaughlin J. L., Hunnicutt D. ( 2001). MtrC, an outer membrane decahaem c cytochrome required for metal reduction in Shewanella putrefaciens MR-1. Mol Microbiol 39:722–730 [View Article][PubMed]
     [Google Scholar]
  7. Bird L. J., Bonnefoy V., Newman D. K. ( 2011). Bioenergetic challenges of microbial iron metabolisms. Trends Microbiol 19:330–340[PubMed] [CrossRef]
     [Google Scholar]
  8. Boogerd F. C., de Vrind J. P. ( 1987). Manganese oxidation by Leptothrix discophora . J Bacteriol 169:489–494[PubMed]
     [Google Scholar]
  9. Borloo J., Vergauwen B., De Smet L., Brigé A., Motte B., Devreese B., Van Beeumen J. ( 2007). A kinetic approach to the dependence of dissimilatory metal reduction by Shewanella oneidensis MR-1 on the outer membrane cytochromes c OmcA and OmcB. FEBS J 274:3728–3738 [View Article][PubMed]
     [Google Scholar]
  10. Bradford M. M. ( 1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254 [View Article][PubMed]
     [Google Scholar]
  11. Bücking C., Popp F., Kerzenmacher S., Gescher J. ( 2010). Involvement and specificity of Shewanella oneidensis outer membrane cytochromes in the reduction of soluble and solid-phase terminal electron acceptors. FEMS Microbiol Lett 306:144–151 [View Article][PubMed]
     [Google Scholar]
  12. Burdige D. J., Nealson K. H. ( 1985). Microbial manganese reduction by enrichment cultures from coastal marine sediments. Appl Environ Microbiol 50:491–497[PubMed]
     [Google Scholar]
  13. Coursolle D., Gralnick J. A. ( 2010). Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1. Mol Microbiol 77:995–1008[PubMed]
     [Google Scholar]
  14. Coursolle D., Baron D. B., Bond D. R., Gralnick J. A. ( 2010). The Mtr respiratory pathway is essential for reducing flavins and electrodes in Shewanella oneidensis . J Bacteriol 192:467–474 [View Article][PubMed]
     [Google Scholar]
  15. Cowan S. W., Schirmer T., Rummel G., Steiert M., Ghosh R., Pauptit R. A., Jansonius J. N., Rosenbusch J. P. ( 1992). Crystal structures explain functional properties of two E. coli porins. Nature 358:727–733 [View Article][PubMed]
     [Google Scholar]
  16. DiChristina T. J., Moore C. M., Haller C. A. ( 2002). Dissimilatory Fe(III) and Mn(IV) reduction by Shewanella putrefaciens requires ferE, a homolog of the pulE (gspE) type II protein secretion gene. J Bacteriol 184:142–151 [View Article][PubMed]
     [Google Scholar]
  17. Dobbin P. S., Warren L. H., Cook N. J., McEwan A. G., Powell A. K., Richardson D. J. ( 1996). Dissimilatory iron(III) reduction by Rhodobacter capsulatus . Microbiology 142:765–774 [View Article]
     [Google Scholar]
  18. El-Naggar M. Y., Wanger G., Leung K. M., Yuzvinsky T. D., Southam G., Yang J., Lau W. M., Nealson K. H., Gorby Y. A. ( 2010). Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1. Proc Natl Acad Sci U S A 107:18127–18131 [View Article][PubMed]
     [Google Scholar]
  19. Emerson D., Fleming E. J., McBeth J. M. ( 2010). Iron-oxidizing bacteria: an environmental and genomic perspective. Annu Rev Microbiol 64:561–583 [View Article][PubMed]
     [Google Scholar]
  20. Firer-Sherwood M. A., Ando N., Drennan C. L., Elliott S. J. ( 2011). Solution-based structural analysis of the decaheme cytochrome, MtrA, by small-angle X-ray scattering and analytical ultracentrifugation. J Phys Chem B 115:11208–11214[PubMed] [CrossRef]
     [Google Scholar]
  21. Francetić O., Pugsley A. P. ( 2005). Towards the identification of type II secretion signals in a nonacylated variant of pullulanase from Klebsiella oxytoca . J Bacteriol 187:7045–7055 [View Article][PubMed]
     [Google Scholar]
  22. Fultz M. L., Durst R. A. ( 1982). Mediator compounds for the electrochemical study of biological redox systems: a compilation. Anal Chim Acta 140:1–18 [View Article]
     [Google Scholar]
  23. Gescher J. S., Cordova C. D., Spormann A. M. ( 2008). Dissimilatory iron reduction in Escherichia coli: identification of CymA of Shewanella oneidensis and NapC of E. coli as ferric reductases. Mol Microbiol 68:706–719 [View Article][PubMed]
     [Google Scholar]
  24. Gibson D. G., Young L., Chuang R. Y., Venter J. C., Hutchison C. A. III, Smith H. O. ( 2009). Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 6:343–345 [View Article][PubMed]
     [Google Scholar]
  25. Gorby Y. A., Yanina S., McLean J. S., Rosso K. M., Moyles D., Dohnalkova A., Beveridge T. J., Chang I. S., Kim B. H. & other authors ( 2006). Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc Natl Acad Sci U S A 103:11358–11363 [View Article][PubMed]
     [Google Scholar]
  26. Gralnick J. A., Vali H., Lies D. P., Newman D. K. ( 2006). Extracellular respiration of dimethyl sulfoxide by Shewanella oneidensis strain MR-1. Proc Natl Acad Sci U S A 103:4669–4674 [View Article][PubMed]
     [Google Scholar]
  27. Hartshorne R. S., Reardon C. L., Ross D., Nuester J., Clarke T. A., Gates A. J., Mills P. C., Fredrickson J. K., Zachara J. M. & other authors ( 2009). Characterization of an electron conduit between bacteria and the extracellular environment. Proc Natl Acad Sci U S A 106:22169–22174 [View Article][PubMed]
     [Google Scholar]
  28. Jiang J., Kappler A. ( 2008). Kinetics of microbial and chemical reduction of humic substances: implications for electron shuttling. Environ Sci Technol 42:3563–3569 [View Article][PubMed]
     [Google Scholar]
  29. Jiao Y., Newman D. K. ( 2007). The pio operon is essential for phototrophic Fe(II) oxidation in Rhodopseudomonas palustris TIE-1. J Bacteriol 189:1765–1773 [View Article][PubMed]
     [Google Scholar]
  30. Jiao Y., Qian F., Li Y., Wang G., Saltikov C. W., Gralnick J. A. ( 2011). Deciphering the electron transport pathway for graphene oxide reduction by Shewanella oneidensis MR-1. J Bacteriol 193:3662–3665 [View Article][PubMed]
     [Google Scholar]
  31. Laemmli U. K. ( 1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685 [View Article][PubMed]
     [Google Scholar]
  32. Li H., Durbin R. ( 2009). Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760 [View Article][PubMed]
     [Google Scholar]
  33. Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R. 1000 Genome Project Data Processing Subgroup ( 2009). The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079 [View Article][PubMed]
     [Google Scholar]
  34. Liu J., Wang Z., Belchik S. M., Edwards M. J., Liu C., Kennedy D. W., Merkley E. D., Lipton M. S., Butt J. N. & other authors ( 2012). Identification and characterization of MtoA: a decaheme c-type cytochrome of the neutrophilic Fe(II)-oxidizing bacterium Sideroxydans lithotrophicus ES-1. Front Microbiol 3:37[PubMed]
     [Google Scholar]
  35. Lovley D. R., Coates J. D., Blunt-Harris E. L., Phillips E. J. P., Woodward J. C. ( 1996). Humic substances as electron acceptors for microbial respiration. Nature 382:445–448 [View Article]
     [Google Scholar]
  36. Lower B. H., Yongsunthon R., Shi L., Wildling L., Gruber H. J., Wigginton N. S., Reardon C. L., Pinchuk G. E., Droubay T. C. & other authors ( 2009). Antibody recognition force microscopy shows that outer membrane cytochromes OmcA and MtrC are expressed on the exterior surface of Shewanella oneidensis MR-1. Appl Environ Microbiol 75:2931–2935 [View Article][PubMed]
     [Google Scholar]
  37. Lutz R., Bujard H. ( 1997). Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements. Nucleic Acids Res 25:1203–1210 [View Article][PubMed]
     [Google Scholar]
  38. Marshall M. J., Beliaev A. S., Dohnalkova A. C., Kennedy D. W., Shi L., Wang Z., Boyanov M. I., Lai B., Kemner K. M. & other authors ( 2006). c-Type cytochrome-dependent formation of U(IV) nanoparticles by Shewanella oneidensis . PLoS Biol 4:e268 [View Article][PubMed]
     [Google Scholar]
  39. Marsili E., Baron D. B., Shikhare I. D., Coursolle D., Gralnick J. A., Bond D. R. ( 2008). Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci U S A 105:3968–3973 [View Article][PubMed]
     [Google Scholar]
  40. Meyer T. E., Tsapin A. I., Vandenberghe I., de Smet L., Frishman D., Nealson K. H., Cusanovich M. A., van Beeumen J. J. ( 2004). Identification of 42 possible cytochrome c genes in the Shewanella oneidensis genome and characterization of six soluble cytochromes. OMICS 8:57–77 [View Article][PubMed]
     [Google Scholar]
  41. Milne I., Bayer M., Cardle L., Shaw P., Stephen G., Wright F., Marshall D. ( 2010). Tablet—next generation sequence assembly visualization. Bioinformatics 26:401–402 [View Article][PubMed]
     [Google Scholar]
  42. Murata T., Tseng W., Guina T., Miller S. I., Nikaido H. ( 2007). PhoPQ-mediated regulation produces a more robust permeability barrier in the outer membrane of Salmonella enterica serovar Typhimurium. J Bacteriol 189:7213–7222 [View Article][PubMed]
     [Google Scholar]
  43. Myers J. M., Myers C. R. ( 2001). Role for outer membrane cytochromes OmcA and OmcB of Shewanella putrefaciens MR-1 in reduction of manganese dioxide. Appl Environ Microbiol 67:260–269 [View Article][PubMed]
     [Google Scholar]
  44. Myers C. R., Myers J. M. ( 2002a). MtrB is required for proper incorporation of the cytochromes OmcA and OmcB into the outer membrane of Shewanella putrefaciens MR-1. Appl Environ Microbiol 68:5585–5594 [View Article][PubMed]
     [Google Scholar]
  45. Myers J. M., Myers C. R. ( 2002b). Genetic complementation of an outer membrane cytochrome omcB mutant of Shewanella putrefaciens MR-1 requires omcB plus downstream DNA. Appl Environ Microbiol 68:2781–2793 [View Article][PubMed]
     [Google Scholar]
  46. Myers J. M., Myers C. R. ( 2003). Overlapping role of the outer membrane cytochromes of Shewanella oneidensis MR-1 in the reduction of manganese(IV) oxide. Lett Appl Microbiol 37:21–25 [View Article][PubMed]
     [Google Scholar]
  47. Myers C. R., Nealson K. H. ( 1988a). Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science 240:1319–1321 [View Article][PubMed]
     [Google Scholar]
  48. Myers C. R., Nealson K. H. ( 1988b). Microbial reduction of manganese oxides: interactions with iron and sulfur. Geochim Cosmochim Acta 52:2727–2732 [View Article]
     [Google Scholar]
  49. Pitts K. E., Dobbin P. S., Reyes-Ramirez F., Thomson A. J., Richardson D. J., Seward H. E. ( 2003). Characterization of the Shewanella oneidensis MR-1 decaheme cytochrome MtrA: expression in Escherichia coli confers the ability to reduce soluble Fe(III) chelates. J Biol Chem 278:27758–27765 [View Article][PubMed]
     [Google Scholar]
  50. Qian Y., Shi L., Tien M. ( 2011a). SO2907, a putative TonB-dependent receptor, is involved in dissimilatory iron reduction by Shewanella oneidensis strain MR-1. J Biol Chem 286:33973–33980 [View Article][PubMed]
     [Google Scholar]
  51. Qian Y., Paquete C. M., Louro R. O., Ross D. E., Labelle E., Bond D. R., Tien M. ( 2011b). Mapping the iron binding site(s) on the small tetraheme cytochrome of Shewanella oneidensis MR-1. Biochemistry 50:6217–6224 [View Article][PubMed]
     [Google Scholar]
  52. Reardon C. L., Dohnalkova A. C., Nachimuthu P., Kennedy D. W., Saffarini D. A., Arey B. W., Shi L., Wang Z., Moore D. & other authors ( 2010). Role of outer-membrane cytochromes MtrC and OmcA in the biomineralization of ferrihydrite by Shewanella oneidensis MR-1. Geobiology 8:56–68 [View Article][PubMed]
     [Google Scholar]
  53. Reguera G., McCarthy K. D., Mehta T., Nicoll J. S., Tuominen M. T., Lovley D. R. ( 2005). Extracellular electron transfer via microbial nanowires. Nature 435:1098–1101 [View Article][PubMed]
     [Google Scholar]
  54. Richter K., Bücking C., Schicklberger M., Gescher J. ( 2010). A simple and fast method to analyze the orientation of c-type cytochromes in the outer membrane of Gram-negative bacteria. J Microbiol Methods 82:184–186 [View Article][PubMed]
     [Google Scholar]
  55. Robie R. A., Huebner J. S., Hemingway B. S. ( 1995). Heat-capacities and thermodynamic properties of braunite (Mn7SiO12) and rhodonite (MnSiO3). Am Mineral 80:560–575
     [Google Scholar]
  56. Roden E. E., Kappler A., Bauer I., Jiang J., Paul A., Stoesser R., Konishi H., Xu H. ( 2010). Extracellular electron transfer through microbial reduction of solid-phase humic substances. Nat Geosci 3:417–421 [View Article]
     [Google Scholar]
  57. Romine M. F., Carlson T. S., Norbeck A. D., McCue L. A., Lipton M. S. ( 2008). Identification of mobile elements and pseudogenes in the Shewanella oneidensis MR-1 genome. Appl Environ Microbiol 74:3257–3265 [View Article][PubMed]
     [Google Scholar]
  58. Ross D. E., Brantley S. L., Tien M. ( 2009). Kinetic characterization of OmcA and MtrC, terminal reductases involved in respiratory electron transfer for dissimilatory iron reduction in Shewanella oneidensis MR-1. Appl Environ Microbiol 75:5218–5226 [View Article][PubMed]
     [Google Scholar]
  59. Saltikov C. W., Newman D. K. ( 2003). Genetic identification of a respiratory arsenate reductase. Proc Natl Acad Sci U S A 100:10983–10988 [View Article][PubMed]
     [Google Scholar]
  60. Sandkvist M. ( 2001). Biology of type II secretion. Mol Microbiol 40:271–283 [View Article][PubMed]
     [Google Scholar]
  61. Schicklberger M., Bücking C., Schuetz B., Heide H., Gescher J. ( 2011). Involvement of the Shewanella oneidensis decaheme cytochrome MtrA in the periplasmic stability of the β-barrel protein MtrB. Appl Environ Microbiol 77:1520–1523 [View Article][PubMed]
     [Google Scholar]
  62. Schuetz B., Schicklberger M., Kuermann J., Spormann A. M., Gescher J. ( 2009). Periplasmic electron transfer via the c-type cytochromes MtrA and FccA of Shewanella oneidensis MR-1. Appl Environ Microbiol 75:7789–7796 [View Article][PubMed]
     [Google Scholar]
  63. Shanks R. M., Caiazza N. C., Hinsa S. M., Toutain C. M., O’Toole G. A. ( 2006). Saccharomyces cerevisiae-based molecular tool kit for manipulation of genes from Gram-negative bacteria. Appl Environ Microbiol 72:5027–5036 [View Article][PubMed]
     [Google Scholar]
  64. Shi L., Chen B., Wang Z., Elias D. A., Mayer M. U., Gorby Y. A., Ni S., Lower B. H., Kennedy D. W. & other authors ( 2006). Isolation of a high-affinity functional protein complex between OmcA and MtrC: two outer membrane decaheme c-type cytochromes of Shewanella oneidensis MR-1. J Bacteriol 188:4705–4714 [View Article][PubMed]
     [Google Scholar]
  65. Shi L., Squier T. C., Zachara J. M., Fredrickson J. K. ( 2007). Respiration of metal (hydr)oxides by Shewanella and Geobacter: a key role for multihaem c-type cytochromes. Mol Microbiol 65:12–20 [View Article][PubMed]
     [Google Scholar]
  66. Shi L., Deng S., Marshall M. J., Wang Z., Kennedy D. W., Dohnalkova A. C., Mottaz H. M., Hill E. A., Gorby Y. A. & other authors ( 2008). Direct involvement of type II secretion system in extracellular translocation of Shewanella oneidensis outer membrane cytochromes MtrC and OmcA. J Bacteriol 190:5512–5516 [View Article][PubMed]
     [Google Scholar]
  67. Shyu J. B., Lies D. P., Newman D. K. ( 2002). Protective role of tolC in efflux of the electron shuttle anthraquinone-2,6-disulfonate. J Bacteriol 184:1806–1810 [View Article][PubMed]
     [Google Scholar]
  68. Spiro T. G., Pape L., Saltman P. ( 1967). Hydrolytic polymerization of ferric citrate. I. Chemistry of polymer. J Am Chem Soc 89:5555–5559 [View Article]
     [Google Scholar]
  69. Stare F. J. ( 1935). A potentiometric study of hepatoflavin. J Biol Chem 112:223–229
     [Google Scholar]
  70. Stevenson F. ( 1994). Humus Chemistry: Genesis, Composition, Reactions New York: Wiley;
     [Google Scholar]
  71. Stookey L. L. ( 1970). Ferrozine—a new spectrophotometric reagent for iron. Anal Chem 42:779–781 [View Article]
     [Google Scholar]
  72. Straub K. L., Benz M., Schink B. ( 2001). Iron metabolism in anoxic environments at near neutral pH. FEMS Microbiol Ecol 34:181–186 [View Article][PubMed]
     [Google Scholar]
  73. Thamdrup B. ( 2000). Bacterial manganese and iron reduction in aquatic sediments. Adv Microb Ecol 16:41–84 [View Article]
     [Google Scholar]
  74. Thomas P. E., Ryan D., Levin W. ( 1976). An improved staining procedure for the detection of the peroxidase activity of cytochrome P-450 on sodium dodecyl sulfate polyacrylamide gels. Anal Biochem 75:168–176 [View Article][PubMed]
     [Google Scholar]
  75. Vaara M. ( 1992). Agents that increase the permeability of the outer membrane. Microbiol Rev 56:395–411[PubMed]
     [Google Scholar]
  76. Venkateswaran K., Moser D. P., Dollhopf M. E., Lies D. P., Saffarini D. A., MacGregor B. J., Ringelberg D. B., White D. C., Nishijima M. & other authors ( 1999). Polyphasic taxonomy of the genus Shewanella and description of Shewanella oneidensis sp. nov.. Int J Syst Bacteriol 49:705–724 [View Article][PubMed]
     [Google Scholar]
  77. von Canstein H., Ogawa J., Shimizu S., Lloyd J. R. ( 2008). Secretion of flavins by Shewanella species and their role in extracellular electron transfer. Appl Environ Microbiol 74:615–623 [View Article][PubMed]
     [Google Scholar]
  78. Xiong Y., Shi L., Chen B., Mayer M. U., Lower B. H., Londer Y., Bose S., Hochella M. F., Fredrickson J. K., Squier T. C. ( 2006). High-affinity binding and direct electron transfer to solid metals by the Shewanella oneidensis MR-1 outer membrane c-type cytochrome OmcA. J Am Chem Soc 128:13978–13979 [View Article][PubMed]
     [Google Scholar]
  79. Zhang H., Tang X., Munske G. R., Zakharova N., Yang L., Zheng C., Wolff M. A., Tolic N., Anderson G. A. & other authors ( 2008). In vivo identification of the outer membrane protein OmcA–MtrC interaction network in Shewanella oneidensis MR-1 cells using novel hydrophobic chemical cross-linkers. J Proteome Res 7:1712–1720 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.058404-0
Loading
Outer-membrane cytochrome-independent reduction of extracellular electron acceptors in Shewanella oneidensis
Microbiology 158, 2144 (2012); https://doi.org/10.1099/mic.0.058404-0
/content/journal/micro/10.1099/mic.0.058404-0
/content/journal/micro/10.1099/mic.0.058404-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error