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Redox-active humics support interspecies syntrophy and shift microbial community

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Abstract

The network of microbial electron transfer can establish a syntrophic association of microbes by connecting interspecies metabolisms, and a variety of redox-active shuttles in environment have been proved to accelerate the electron flow in a microbial community. Using humic substances as models, we investigated how different redox-active shuttles with different electrochemical properties influence interspecies electron transfer, and affect the shift of microbial communities. The co-culture of two species was constructed with supplements of humics, and the electron transfer between these two strains was found to be linked by humic acid with a wider window of redox potential and multi-peaks of redox reactions. Based on the shift of microbial composition, the humic substances with a wide potential window and multi-peaks of redox reactions for accepting and donating electrons could increase the biodiversity (Chao 1 and phylogenetic diversity) with a large extent. The mechanism by which redox-active shuttles mediate the microbial electron transfer network could facilitate our understanding of syntrophic interactions between microbes.

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References

  1. Jackson B E, McInerney M J. Anaerobic microbial metabolism can proceed close to thermodynamic limits. Nature, 2002, 415: 454–456

    Article  Google Scholar 

  2. Wegener G, Krukenberg V, Riedel D, et al. Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria. Nature, 2015, 526: 587–590

    Article  Google Scholar 

  3. Nielsen L P, Risgaard-Petersen N, Fossing H, et al. Electric currents couple spatially separated biogeochemical processes in marine sediment. Nature, 2010, 463: 1071–1074

    Article  Google Scholar 

  4. Pfeffer C, Larsen S, Song J, et al. Filamentous bacteria transport electrons over centimetre distances. Nature, 2012, 491: 218–221

    Article  Google Scholar 

  5. Wan Y, Zhou L, Wang S, et al. Syntrophic growth of Geobacter sulfurreducens accelerates anaerobic denitrification. Front Microbiol, 2018, 9: 1572

    Article  Google Scholar 

  6. Lovley D R. Powering microbes with electricity: Direct electron transfer from electrodes to microbes. Environ MicroBiol Rep, 2011, 3: 27–35

    Article  Google Scholar 

  7. Reguera G, McCarthy K D, Mehta T, et al. Extracellular electron transfer via microbial nanowires. Nature, 2005, 435: 1098–1101

    Article  Google Scholar 

  8. Marsili E, Baron D B, Shikhare I D, et al. Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci USA, 2008, 105: 3968–3973

    Article  Google Scholar 

  9. Zheng Y, Huang J, Zhao F, et al. Physiological effect of XoxG(4) on lanthanide-dependent methanotrophy. mBio, 2018, 9: e02430-17–2417

    Article  Google Scholar 

  10. Milucka J, Ferdelman T G, Polerecky L, et al. Zero-valent sulphur is a key intermediate in marine methane oxidation. Nature, 2012, 491: 541–546

    Article  Google Scholar 

  11. Lohmayer R, Kappler A, Lösekann-Behrens T, et al. Sulfur species as redox partners and electron shuttles for ferrihydrite reduction by Sulfurospirillum deleyianum. Appl Environ Microbiol, 2014, 80: 3141–3149

    Article  Google Scholar 

  12. Liu F, Rotaru A E, Shrestha P M, et al. Promoting direct interspecies electron transfer with activated carbon. Energy Environ Sci, 2012, 5: 8982–8989

    Article  Google Scholar 

  13. Kato S, Hashimoto K, Watanabe K. Microbial interspecies electron transfer via electric currents through conductive minerals. Proc Natl Acad Sci USA, 2012, 109: 10042–10046

    Article  Google Scholar 

  14. Lovley D R, Coates J D, Blunt-Harris E L, et al. Humic substances as electron acceptors for microbial respiration. Nature, 1996, 382: 445–448

    Article  Google Scholar 

  15. Stams A J M, Plugge C M. Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat Rev Micro, 2009, 7: 568–577

    Article  Google Scholar 

  16. Shrestha P M, Rotaru A E. Plugging in or going wireless: Strategies for interspecies electron transfer. Front Microbiol, 2014, 5: 237

    Google Scholar 

  17. Hedges J I, Eglinton G, Hatcher P G, et al. The molecularly-uncharacterized component of nonliving organic matter in natural environments. Org GeoChem, 2000, 31: 945–958

    Article  Google Scholar 

  18. Voelker B M, Morel F M M, Sulzberger B. Iron redox cycling in surface waters: Effects of humic substances and light. Environ Sci Technol, 1997, 31: 1004–1011

    Article  Google Scholar 

  19. Aeschbacher M, Brunner S H, Schwarzenbach R P, et al. Assessing the effect of humic acid redox state on organic pollutant sorption by combined electrochemical reduction and sorption experiments. Environ Sci Technol, 2012, 46: 3882–3890

    Article  Google Scholar 

  20. Lovley D R, Fraga J L, Coates J D, et al. Humics as an electron donor for anaerobic respiration. Environ Microbiol, 1999, 1: 89–98

    Article  Google Scholar 

  21. Van Trump J I, Wrighton K C, Thrash J C, et al. Humic acid-oxidizing, nitrate-reducing bacteria in agricultural soils. mBio, 2011, 2: e00044

    Google Scholar 

  22. Cervantes F J, Bok F A M, Duong-Dac T, et al. Reduction of humic substances by halorespiring, sulphate-reducing and methanogenic microorganisms. Environ Microbiol, 2002, 4: 51–57

    Google Scholar 

  23. Klüpfel L, Piepenbrock A, Kappler A, et al. Humic substances as fully regenerable electron acceptors in recurrently anoxic environments. Nat Geosci, 2014, 7: 195–200

    Article  Google Scholar 

  24. Zhou S, Chen S, Yuan Y, et al. Influence of Humic acid complexation with metal ions on extracellular electron transfer activity. Sci Rep, 2015, 5: 17067

    Article  Google Scholar 

  25. Smith J A, Nevin K P, Lovley D R. Syntrophic growth via quinonemediated interspecies electron transfer. Front Microbiol, 2015, 6: 121

    Google Scholar 

  26. Scott D T, McKnight D M, Blunt-Harris E L, et al. Quinone moieties act as electron acceptors in the reduction of humic substances by humics-reducing microorganisms. Environ Sci Technol, 1999, 33: 372

    Article  Google Scholar 

  27. Sharpless C M, Aeschbacher M, Page S E, et al. Photooxidationinduced changes in optical, electrochemical, and photochemical properties of humic substances. Environ Sci Technol, 2014, 48: 2688–2696

    Article  Google Scholar 

  28. Caccavo F, Lonergan D J, Lovley D R, et al. Geobacter sulfurreducens sp. nov., a hydrogen-and acetate-oxidizing dissimilatory metal-reducing microorganism. App Environ Microbiol, 1994, 60: 3752–3759

    Google Scholar 

  29. Beller H R, Chain P S G, Letain T E, et al. The genome sequence of the obligately chemolithoautotrophic, facultatively anaerobic bacterium Thiobacillus denitrificans. J Bacteriology, 2006, 188: 1473–1488

    Article  Google Scholar 

  30. Kato S, Nakamura R, Kai F, et al. Respiratory interactions of soil bacteria with (semi)conductive iron-oxide minerals. Environ Micro- Biol, 2010, 12: 3114–3123

    Article  Google Scholar 

  31. Zheng Y, Wang C, Zheng Z Y, et al. Ameliorating acidic soil using bioelectrochemistry systems. RSC Adv, 2014, 4: 62544–62549

    Article  Google Scholar 

  32. Zheng Y, Xiao Y, Yang Z H, et al. The bacterial communities of bioelectrochemical systems associated with the sulfate removal under different pHs. Process Biochem, 2014, 49: 1345–1351

    Article  Google Scholar 

  33. Nurmi J T, Tratnyek P G. Electrochemical properties of natural organic matter (NOM), fractions of NOM, and model biogeochemical electron shuttles. Environ Sci Technol, 2002, 36: 617–624

    Article  Google Scholar 

  34. Wu S, Fang G, Wang Y, et al. Redox-active oxygen-containing functional groups in activated carbon facilitate microbial reduction of ferrihydrite. Environ Sci Technol, 2018, 51: 9709–9717

    Article  Google Scholar 

  35. Spain A M, Krumholz L R, Elshahed M S. Abundance, composition, diversity and novelty of soil Proteobacteria. ISME J, 2009, 3: 992–1000

    Article  Google Scholar 

  36. Falkowski P G, Fenchel T, Delong E F. The microbial engines that drive earth’s biogeochemical cycles. Science, 2008, 320: 1034–1039

    Article  Google Scholar 

  37. Cai Q, Yuan Y, Hu P, et al. Progress in study of humic substances: electrochemical redox characterization and extracellular respiration. Chin J Appl Environ Biol, 2015: 996–1002

    Google Scholar 

  38. Rotaru A E, Shrestha P M, Liu F, et al. Direct interspecies electron transfer between Geobacter metallireducens and Methanosarcina barkeri. Appl Environ Microbiol, 2014, 80: 4599–4605

    Article  Google Scholar 

  39. Chen S, Rotaru A E, Shrestha P M, et al. Promoting interspecies electron transfer with biochar. Sci Rep, 2015, 4: 5019

    Article  Google Scholar 

  40. Van der Zee F P, Cervantes F J. Impact and application of electron shuttles on the redox (bio)transformation of contaminants: A review. Biotech Adv, 2009, 27: 256–277

    Article  Google Scholar 

  41. Kato S, Hashimoto K, Watanabe K. Methanogenesis facilitated by electric syntrophy via (semi)conductive iron-oxide minerals. Environ MicroBiol, 2012, 14: 1646–1654

    Article  Google Scholar 

  42. Huang L, Angelidaki I. Effect of humic acids on electricity generation integrated with xylose degradation in microbial fuel cells. Biotechnol Bioeng, 2008, 100: 413–422

    Article  Google Scholar 

  43. Torsvik V, Øvreås L. Microbial diversity and function in soil: From genes to ecosystems. Curr Opin MicroBiol, 2002, 5: 240–245

    Article  Google Scholar 

  44. Watanabe K, Manefield M, Lee M, et al. Electron shuttles in biotechnology. Curr Opin Biotech, 2009, 20: 633–641

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (Grant Nos. 41471260, 21777155). We would like to thank Ellen Struve and Wiebke Ruschmeier at University of Tuebingen for the suggestions of experimental techniques.

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Authors and Affiliations

  1. CAS Key Laboratory of Urban Pollutant Conversion, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, 361021, China

    Yue Zheng, Yong Xiao, Fan Yang, Gurumurthy Dummi Mahadeva & Feng Zhao

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Yue Zheng & Fan Yang

  3. Geomicrobiology, Center for Applied Geosciences, University of Tuebingen, Tuebingen, 72076, Germany

    Andreas Kappler

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  1. Yue Zheng
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  2. Andreas Kappler
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  3. Yong Xiao
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  4. Fan Yang
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  5. Gurumurthy Dummi Mahadeva
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  6. Feng Zhao
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Correspondence to Feng Zhao.

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Zheng, Y., Kappler, A., Xiao, Y. et al. Redox-active humics support interspecies syntrophy and shift microbial community. Sci. China Technol. Sci. 62, 1695–1702 (2019). https://doi.org/10.1007/s11431-018-9360-5

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  • DOI: https://doi.org/10.1007/s11431-018-9360-5

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