Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Light-independent anaerobic microbial oxidation of manganese driven by an electrosyntrophic coculture

The ISME Journal volume 17, pages 163–171 (2023)Cite this article

Subjects

Abstract

Anaerobic microbial manganese oxidation (AMMO) has been considered an ancient biological metabolism for Mn element cycling on Archaean Earth before the presence of oxygen. A light-dependent AMMO was recently observed under strictly anoxic conditions, providing a new proxy for the interpretation of the evolution of oxygenic photosynthesis. However, the feasibility of biotic Mn(II) oxidation in dark geological habitats that must have been abundant remains unknown. Therefore, we discovered that it would be possible to achieve AMMO in a light-independent electrosyntrophic coculture between Rhodopseudomonas palustris and Geobacter metallireducens. Transmission electron microscopy analysis revealed insoluble particle formation in the coculture with Mn(II) addition. X-ray diffraction and X-ray photoelectron spectroscopy analysis verified that these particles were a mixture of MnO2 and Mn3O4. The absence of Mn oxides in either of the monocultures indicated that the Mn(II)-oxidizing activity was induced via electrosyntrophic interactions. Radical quenching and isotopic experiments demonstrated that hydroxyl radicals (•OH) produced from H2O dissociation by R. palustris in the coculture contributed to Mn(II) oxidation. All these findings suggest a new, symbiosis-dependent and light-independent AMMO route, with potential importance to the evolution of oxygenic photosynthesis and the biogeochemical cycling of manganese on Archaean and modern Earth.

This is a preview of subscription content, access via your institution

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

Buy

All prices are NET prices.

Fig. 1: Manganese oxide formation in electrosyntrophic cocultures of G. metallireducens and R. palustris.
Fig. 2: Characteristics of insoluble manganese oxides.
Fig. 3: ROS generation in G. metallireducens and R. palustris cocultures.
Fig. 4: •OH identification and mass spectra of DMPO/•OH in G. metallireducens and R. palustris cocultures.
Fig. 5: Strategy of light-independent AMMO in G. metallireducens and R. palustris cocultures under dark and anoxic conditions.

Data availability

All data are available in the main text or the Supplementary Materials. Additional data related to this paper may be requested from the authors.

References

  1. Gounot AM. Microbial oxidation and reduction of manganese: consequences in groundwater and applications. FEMS Microbiol Rev. 1994;14:339–49.

    Article  CAS  Google Scholar 

  2. Roels HA, Bowler RM, Kim Y, Claus HB, Mergler D, Hoet P, et al. Manganese exposure and cognitive deficits: a growing concern for manganese neurotoxicity. Neurotoxicology. 2012;33:872–80.

    Article  CAS  Google Scholar 

  3. Zhou H, Fu C. Manganese-oxidizing microbes and biogenic manganese oxides: characterization, Mn(II) oxidation mechanism and environmental relevance. Rev Environ Sci Bio. 2020;19:489–507.

    Article  CAS  Google Scholar 

  4. Butterfield CN, Soldatova AV, Lee SW, Spiro TG, Tebo BM. Mn(II, III) oxidation and MnO2 mineralization by an expressed bacterial multicopper oxidase. Proc Natl Acad Sci USA. 2013;110:11731–5.

    Article  CAS  Google Scholar 

  5. Anderson CR, Johnson HA, Caputo N, Davis RE, Torpey JW, Tebo BM. Mn(II) oxidation is catalyzed by heme peroxidases in Aurantimonas manganoxydans strain SI85-9A1 and Erythrobacter sp. strain SD-21. Appl Environ Microbiol. 2009;75:4130–8.

    Article  CAS  Google Scholar 

  6. Hansel CM, Zeiner CA, Santelli CM, Webb SM. Mn(II) oxidation by an ascomycete fungus is linked to superoxide production during asexual reproduction. Proc Natl Acad Sci USA. 2012;109:12621–5.

    Article  CAS  Google Scholar 

  7. Learman DR, Voelker BM, Vazquez-Rodriguez AI, Hansel CM. Formation of manganese oxides by bacterially generated superoxide. Nat Geosci 2011;4:95–98.

    Article  CAS  Google Scholar 

  8. Yu H, Leadbetter JR. Bacterial chemolithoautotrophy via manganese oxidation. Nature. 2020;583:453–8.

    Article  CAS  Google Scholar 

  9. Planavsky NJ, Asael D, Hofmann A, Reinhard CT, Lalonde SV, Knudsen A, et al. Evidence for oxygenic photosynthesis half a billion years before the Great Oxidation Event. Nat Geosci. 2014;7:283–6.

    Article  CAS  Google Scholar 

  10. Bontognali TRR. Anoxygenic phototrophs and the forgotten art of making dolomite. Geology. 2019;47:591–2.

    Article  Google Scholar 

  11. Daye M, Higgins J, Bosak T. Formation of ordered dolomite in anaerobic photosynthetic biofilms. Geology. 2019;47:509–12.

    Article  CAS  Google Scholar 

  12. Liu W, Hao J, Elzinga EJ, Piotrowiak P, Nanda V, Yee N, et al. Anoxic photogeochemical oxidation of manganese carbonate yields manganese oxide. Proc Natl Acad Sci USA. 2020;117:22698–704.

    Article  CAS  Google Scholar 

  13. Daye M, Klepac-Ceraj V, Pajusalu M, Rowland S, Farrell-Sherman A, Beukes N, et al. Light-driven anaerobic microbial oxidation of manganese. Nature. 2019;576:311–4.

    Article  Google Scholar 

  14. Yang P, Tan GYA, Aslam M, Kim J, Lee PH. Metatranscriptomic evidence for classical and RuBisCO-mediated CO2 reduction to methane facilitated by direct interspecies electron transfer in a methanogenic system. Sci Rep. 2019;9:4116.

    Article  Google Scholar 

  15. Ha PT, Lindemann SR, Shi L, Dohnalkova AC, Fredrickson JK, Madigan MT, et al. Syntrophic anaerobic photosynthesis via direct interspecies electron transfer. Nat Commun. 2017;8:13924.

    Article  CAS  Google Scholar 

  16. Nagarajan H, Embree M, Rotaru AE, Shrestha PM, Feist AM, Palsson BØ, et al. Characterization and modelling of interspecies electron transfer mechanisms and microbial community dynamics of a syntrophic association. Nat Commun. 2013;4:2809.

    Article  Google Scholar 

  17. Summers ZM, Fogarty HE, Leang C, Franks AE, Malvankar NS, Lovley DR. Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria. Science. 2010;330:1413–5.

    Article  CAS  Google Scholar 

  18. Rotaru AE, Shrestha PM, Liu F, Markovaite B, Chen S, Nevin KP, et al. Direct interspecies electron transfer between Geobacter metallireducens and Methanosarcina barkeri. Appl Environ Microbiol. 2014;80:4599–605.

    Article  Google Scholar 

  19. Boone DR, Johnson RL, Liu Y. Diffusion of the interspecies electron carriers H2 and formate in methanogenic ecosystems and its implications in the measurement of Km for H2 or formate uptake. Appl Environ Microbiol. 1989;55:1735–41.

    Article  CAS  Google Scholar 

  20. Guzman MS, Rengasamy K, Binkley MM, Jones C, Ranaivoarisoa TO, Singh R, et al. Phototrophic extracellular electron uptake is linked to carbon dioxide fixation in the bacterium Rhodopseudomonas palustris. Nat Commun. 2019;10:1355.

    Article  Google Scholar 

  21. Liu X, Huang L, Rensing C, Ye J, Nealson KH, Zhou S. Syntrophic interspecies electron transfer drives carbon fixation and growth by Rhodopseudomonas palustris under dark, anoxic conditions. Sci Adv. 2021;7:eabh1852.

    Article  CAS  Google Scholar 

  22. Allen JP, Olson TL, Oyala P, Lee WJ, Tufts AA, Williams JC. Light-driven oxygen production from superoxide by Mn-binding bacterial reaction centers. Proc Natl Acad Sci USA. 2012;109:2314–8.

    Article  CAS  Google Scholar 

  23. Huang L, Liu X, Zhang Z, Ye J, Rensing C, Zhou S, et al. Light-driven carbon dioxide reduction to methane by Methanosarcina barkeri in an electric syntrophic coculture. ISME J. 2022;16:370–7.

    Article  CAS  Google Scholar 

  24. Huang L, Liu X, Ye Y, Chen M, Zhou S. Evidence for the coexistence of direct and riboflavin-mediated interspecies electron transfer in Geobacter coculture. Environ Microbiol. 2020;22:243–54.

    Article  CAS  Google Scholar 

  25. Liu X, Zhuo S, Rensing C, Zhou S. Syntrophic growth with direct interspecies electron transfer between pili-free Geobacter species. ISME J 2018;12:2142–51.

    Article  CAS  Google Scholar 

  26. Chen M, Zhou XF, Yu YQ, Liu X, Zeng RJ, Zhou SG, et al. Light-driven nitrous oxide production via autotrophic denitrification by self-photosensitized Thiobacillus denitrificans. Environ Int 2019;127:353–60.

    Article  CAS  Google Scholar 

  27. Richardson L, Aguilar C, Nealson K. Manganese oxidation in pH and O2 microenvironments produced by phytoplankton. Limnol oceanogr 1988;33:352–63.

    Article  CAS  Google Scholar 

  28. Chen M, Zhou X, Chen X, Cai Q, Zeng RJ, Zhou S. Mechanisms of nitrous oxide emission during photoelectrotrophic denitrification by self-photosensitized Thiobacillus denitrificans. Water Res. 2020;172:115501.

    Article  CAS  Google Scholar 

  29. Choi HS, Kim JW, Cha YN, Kim C. A quantitative nitroblue tetrazolium assay for determining intracellular superoxide anion production in phagocytic cells. J Immunoass Immunochem. 2006;27:31–44.

    Article  CAS  Google Scholar 

  30. Chen X, Feng Q, Cai Q, Huang S, Yu Y, Zeng RJ, et al. Mn3O4 nanozyme coating accelerates nitrate reduction and decreases N2O emission during photoelectrotrophic denitrification by Thiobacillus denitrificans-CdS. Environ Sci Technol. 2020;54:10820–30.

    Article  CAS  Google Scholar 

  31. Barreto JC, Smith GS, Strobel NH, McQuillin PA, Miller TA. Terephthalic acid: a dosimeter for the detection of hydroxyl radicals in vitro. Life Sci. 1995;56:89–96.

    Article  Google Scholar 

  32. Huang L, Liu X, Tang J, Yu L, Zhou S. Electrochemical evidence for direct interspecies electron transfer between Geobacter sulfurreducens and Prosthecochloris aestuarii. Bioelectrochemistry. 2019;127:21–25.

    Article  CAS  Google Scholar 

  33. Bonini MG, Miyamoto S, Mascio PD, Augusto O. Production of the carbonate radical anion during xanthine oxidase turnover in the presence of bicarbonate. J Biol Chem. 2004;279:51836–43.

    Article  CAS  Google Scholar 

  34. Ju W, Jin B, Dong C, Wen Z, Jiang Q. Rice-shaped Fe2O3@C@Mn3O4 with three-layer core-shell structure as a high-performance anode for lithium-ion batteries. J Electroanal Chem. 2020;861:113942.

    Article  CAS  Google Scholar 

  35. Wang HY, Li DG, Zhu HL, Qi YX, Li H, Lun N, et al. Mn3O4/Ni(OH)2 nanocomposite as an applicable electrode material for pseudocapacitors. Electrochim Acta. 2017;249:155–65.

    Article  CAS  Google Scholar 

  36. Moses Ezhil Raj A, Victoria SG, Jothy VB, Ravidhas C, Wollschläger J, Suendorf M, et al. XRD and XPS characterization of mixed valence Mn3O4 hausmannite thin films prepared by chemical spray pyrolysis technique. Appl Surf Sci. 2010;256:2920–6.

    Article  CAS  Google Scholar 

  37. Qiu W, Lin Z, Xiao H, Zhang G, Gao H, Feng H, et al. Construction of chemical self-charging zinc ion batteries based on defect coupled nitrogen modulation of zinc manganite vertical graphene arrays. Mater Adv. 2021;2:6694–702.

    Article  CAS  Google Scholar 

  38. Yao B, Xiao T, Makgae OA, Jie X, Gonzalez-Cortes S, Guan S, et al. Transforming carbon dioxide into jet fuel using an organic combustion-synthesized Fe-Mn-K catalyst. Nat Commun 2020;11:6395.

    Article  CAS  Google Scholar 

  39. Chigane M, Ishikawa M. Manganese oxide thin film preparation by potentiostatic electrolyses and electrochromism. J Electrochem Soc. 2000;147:6.

    Article  Google Scholar 

  40. Fischer WW, Hemp J, Johnson JE. Manganese and the evolution of photosynthesis. Orig Life Evol B. 2015;45:351–7.

    Article  CAS  Google Scholar 

  41. Liang J, Bai Y, Men Y, Qu J. Microbe-microbe interactions trigger Mn(II)-oxidizing gene expression. ISME J. 2017;11:67–77.

    Article  CAS  Google Scholar 

  42. Reynard D, Maye S, Peljo P, Chanda V, Girault HH, Gentil S. Vanadium-manganese redox flow battery: study of Mn(III) disproportionation in the oresence of other metallic ions. Chemistry. 2020;26:7250–7.

    Article  CAS  Google Scholar 

  43. Zhang B, Sun L. Why nature chose the Mn4CaO5 cluster as water-splitting catalyst in photosystem II: a new hypothesis for the mechanism of O-O bond formation. Dalton Trans. 2018;47:14381–7.

    Article  CAS  Google Scholar 

  44. Hansel CM, Francis CA. Coupled photochemical and enzymatic Mn(II) oxidation pathways of a planktonic Roseobacter-Like bacterium. Appl Environ Microbiol. 2006;72:3543–9.

    Article  CAS  Google Scholar 

  45. Learman D, Voelker B, Madden A, Hansel C. Constraints on superoxide mediated formation of manganese oxides. Front Microbiol. 2013;4:262.

    Article  Google Scholar 

  46. Du X, Oturan MA, Zhou M, Belkessa N, Su P, Cai J, et al. Nanostructured electrodes for electrocatalytic advanced oxidation processes: from materials preparation to mechanisms understanding and wastewater treatment applications. Appl Catal B-Environ. 2021;296:120332.

    Article  CAS  Google Scholar 

  47. Wang X, Zhang L. Kinetic study of hydroxyl radical formation in a continuous hydroxyl generation system. RSC Adv. 2018;8:40632–8.

    Article  CAS  Google Scholar 

  48. Cao W, Jin M, Yang K, Chen B, Xiong M, Li X, et al. Fenton/Fenton-like metal-based nanomaterials combine with oxidase for synergistic tumor therapy. J Nanobiotechnol. 2021;19:325.

    Article  CAS  Google Scholar 

  49. Benon HJB, Cabelli DE Superoxide and hydroxyl radical chemistry in aqueous solution. Springer Netherlands 1995.

  50. Hussain S, Ali SF. Manganese scavenges superoxide and hydroxyl radicals: an in vitro study in rats. Neurosci Lett. 1999;261:21–24.

    Article  CAS  Google Scholar 

  51. Méndez-Alvarez E, Soto-Otero R, Hermida-Ameijeiras A, López-Martín ME, Labandeira-García JL. Effect of iron and manganese on hydroxyl radical production by 6-hydroxydopamine: mediation of antioxidants. Free Radic Bio Med. 2001;31:986–98.

    Article  Google Scholar 

  52. Slimen IB, Najar T, Ghram A, Dabbebi H, Ben Mrad M, Abdrabbah M. Reactive oxygen species, heat stress and oxidative-induced mitochondrial damage: a review. Int J Hyperther. 2014;30:513–23.

    Article  Google Scholar 

  53. Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol. 2003;552:335–44.

    Article  CAS  Google Scholar 

  54. Siahrostami S, Li GL, Viswanathan V, Nørskov JK. One- or two-electron water oxidation, hydroxyl radical, or H2O2 evolution. J Phys Chem Lett. 2017;8:1157–60.

    Article  CAS  Google Scholar 

  55. Ling C, Liu X, Li M, Wang X, Shi Y, Qi J, et al. Sulphur vacancy derived anaerobic hydroxyl radical generation at the pyrite-water interface: pollutants removal and pyrite self-oxidation behavior. Appl Catal B-Environ. 2021;290:120051.

    Article  CAS  Google Scholar 

  56. Su JF, Zheng SC, Huang TL, Ma F, Shao SC, Yang SF, et al. Simultaneous removal of Mn(II) and nitrate by the manganese-oxidizing bacterium Acinetobacter sp. SZ28 in anaerobic conditions. Geomicrobiol J. 2016;33:586–91.

    Article  CAS  Google Scholar 

  57. Shen G, Golbeck JH Assembly of the bound iron-sulfur clusters in photosystem I. Springer Netherlands 2006:529-48.

  58. Beinert H, Kennedy MC, Stout CD. Aconitase as ironminus signsulfur protein, enzyme, and iron-regulatory protein. Chem Rev 1996;96:2335–74.

    Article  CAS  Google Scholar 

  59. Jin Z, Heinnickel M, Krebs C, Shen G, Golbeck JH, Bryant DA.Biogenesis of iron-sulfur clusters in photosystem I: holo-NfuA from the cyanobacterium Synechococcus sp. PCC 7002 rapidly and efficiently transfers [4Fe-4S] clusters to apo-PsaC in vitro. J Biol Chem. 2008;283:28426–35.

    Article  CAS  Google Scholar 

  60. Boyd ES, Thomas KM, Dai Y, Boyd JM, Outten FW. Interplay between oxygen and Fe–S cluster biogenesis: insights from the Suf pathway. Biochemistry. 2014;53:5834–47.

    Article  CAS  Google Scholar 

  61. Boesen T, Nielsen LP, Schramm A. Pili for nanowires. Nat Microbiol. 2021;6:1347–8.

    Article  CAS  Google Scholar 

  62. Shi L, Dong H, Reguera G, Beyenal H, Lu A, Liu J, et al. Extracellular electron transfer mechanisms between microorganisms and minerals. Nat Rev Microbiol. 2016;14:651–62.

    Article  CAS  Google Scholar 

  63. Hullar T, Anastasio C. Yields of hydrogen peroxide from the reaction of hydroxyl radical with organic compounds in solution and ice. Atmos Chem Phys 2011;11:7209.

    Article  CAS  Google Scholar 

  64. Stemmler K, von Gunten U. OH radical-initiated oxidation of organic compounds in atmospheric water phases: part 1. Reactions of peroxyl radicals derived from 2-butoxyethanol in water. Atmos Environ. 2000;34:4241–52.

    Article  CAS  Google Scholar 

  65. Yuan C, Chin YP, Weavers LK. Photochemical acetochlor degradation induced by hydroxyl radical in Fe-amended wetland waters: impact of pH and dissolved organic matter. Water Res. 2018;132:52–60.

    Article  CAS  Google Scholar 

  66. Liao P, Yu K, Lu Y, Wang P, Liang Y, Shi Z. Extensive dark production of hydroxyl radicals from oxygenation of polluted river sediments. Chem Eng J 2019;368:700–9.

    Article  CAS  Google Scholar 

  67. Wan D, Liu FF, Chen JB, Kappler A, Kuzyakov Y, Liu CQ, et al. Microbial community mediates hydroxyl radical production in soil slurries by iron redox transformation. Water Res. 2022;220:118689.

    Article  CAS  Google Scholar 

  68. Brezonik PL, Fulkerson-Brekken J. Nitrate-induced photolysis in natural waters: controls on concentrations of hydroxyl radical photo-intermediates by natural scavenging agents. Environ Sci Technol. 1998;32:3004–10.

    Article  CAS  Google Scholar 

  69. Ou Y, Wu J, Meyer JR, Foston M, Fortner JD, Li W. Photoenhanced oxidation of nC60 in water: exploring H2O2 and hydroxyl radical based reactions. Chem Eng J. 2019;360:665–72.

    Article  CAS  Google Scholar 

  70. Aguirre J, Ríos-Momberg M, Hewitt D, Hansberg W. Reactive oxygen species and development in microbial eukaryotes. Trends Microbiol. 2005;13:111–8.

    Article  CAS  Google Scholar 

  71. Zhang T, Hansel CM, Voelker BM, Lamborg CH. Extensive dark biological production of reactive oxygen species in brackish and freshwater ponds. Environ Sci Technol. 2016;50:2983–93.

    Article  CAS  Google Scholar 

  72. Page SE, Kling GW, Sander M, Harrold KH, Logan JR, McNeill K, et al. Dark formation of hydroxyl radical in Arctic soil and surface waters. Environ Sci Technol. 2013;47:12860–7.

    Article  CAS  Google Scholar 

  73. Tong M, Yuan S, Ma S, Jin M, Liu D, Cheng D, et al. Production of abundant hydroxyl radicals from oxygenation of subsurface sediments. Environ Sci Technol. 2016;50:214–21.

    Article  CAS  Google Scholar 

  74. Schaefer CE, Ho P, Berns E, Werth C. Mechanisms for abiotic dechlorination of trichloroethene by ferrous minerals under oxic and anoxic conditions in natural sediments. Environ Sci Technol. 2018;52:13747–55.

    Article  CAS  Google Scholar 

  75. Pospíšil P, Arató A, Krieger-Liszkay A, Rutherford AW. Hydroxyl radical generation by photosystem II. Biochemistry. 2004;43:6783–92.

    Article  Google Scholar 

  76. Minella M, De Laurentiis E, Maurino V, Minero C, Vione D. Dark production of hydroxyl radicals by aeration of anoxic lake water. Sci Total Environ 2015;527-528:322–7.

    Article  CAS  Google Scholar 

  77. Wang W, Fan W, Huo M, Zhao H, Lu Y. Hydroxyl radical generation and contaminant removal from water by the collapse of microbubbles under different hydrochemical conditions. Water Air Soil Poll. 2018;229:86.

    Article  Google Scholar 

  78. Chernev P, Fischer S, Hoffmann J, Oliver N, Assunção R, Yu B, et al. Light-driven formation of manganese oxide by today’s photosystem II supports evolutionarily ancient manganese-oxidizing photosynthesis. Nat Commun. 2020;11:6110.

    Article  CAS  Google Scholar 

  79. Elsner RJ, Spangler JG. Neurotoxicity of inhaled manganese: public health danger in the shower? Med Hypotheses. 2005;65:607–16.

    Article  CAS  Google Scholar 

  80. Frantz OO, Hofmann A, Wille M, Spangenberg JE, Bekker A, Poulton SW, et al. Aerobic iron and manganese cycling in a redox-stratified Mesoarchean epicontinental sea. Earth Planet Sci Lett. 2018;500:28–40.

    Article  Google Scholar 

  81. Baturin GN The geochemistry of manganese and manganese nodules in the ocean, GN Baturin, Ed. (Springer Netherlands, Dordrecht, 1988), pp. 58-82.

  82. Calvert SE, Pedersen TF. Sedimentary geochemistry of manganese; implications for the environment of formation of manganiferous black shales. Econ Geol. 1996;91:36–47.

    Article  CAS  Google Scholar 

  83. Miyata N, Tani Y, Sakata M, Iwahori K. Microbial manganese oxide formation and interaction with toxic metal ions. J Biosci Bioeng. 2007;104:1–8.

    Article  CAS  Google Scholar 

  84. Wang Y, Stone AT. Reaction of Mn(III,IV) (hydr)oxides with oxalic acid, glyoxylic acid, phosphonoformic acid, and structurally-related organic compounds. Geochim Cosmochim Acta. 2006;70:4477–90.

    Article  CAS  Google Scholar 

  85. Lu A, Li Y, Liu F, Liu Y, Ye H, Zhuang Z, et al. The photogeochemical cycle of Mn oxides on the Earth’s surface. Mineral Mag. 2021;85:22–38.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China, Grant no. 42177270 and 42077218, the China Postdoctoral Science Foundation, grant no. 2021M700879, Guangdong Basic and Applied Basic Research Foundation, Grant no. 2021A1515110918.

Author information

Author notes

  1. These authors contributed equally: Lingyan Huang, Xing Liu.

Authors and Affiliations

  1. Guangdong Key Laboratory of Environmental Catalysis and Health Risk Control, School of Environmental Science and Engineering, Institute of Environmental Health and Pollution Control, Guangdong University of Technology, Guangzhou, China

    Lingyan Huang & Yong Yuan

  2. Fujian Provincial Key Laboratory of Soil Environmental Health and Regulation, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, China

    Lingyan Huang, Xing Liu, Christopher Rensing & Shungui Zhou

  3. Department of Earth Science, University of Southern California, Los Angeles, CA, USA

    Kenneth H. Nealson

Authors
  1. Lingyan Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xing Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christopher Rensing
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yong Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shungui Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kenneth H. Nealson
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

LH, XL, YY, and SZ conceived and designed the study; LH performed the experiments, collected the data, and drew all figures. YY and XL wrote the manuscript; XL, YY, CR, SZ, and KN analyzed and interpreted the data; CR and KN revised the manuscript. All authors reviewed, revised, and approved the final manuscript.

Corresponding author

Correspondence to Yong Yuan.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Huang, L., Liu, X., Rensing, C. et al. Light-independent anaerobic microbial oxidation of manganese driven by an electrosyntrophic coculture. ISME J 17, 163–171 (2023). https://doi.org/10.1038/s41396-022-01335-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41396-022-01335-3

Search

Advanced search

Quick links