Skip to main content
SpringerLink
Log in

Anodic microbial community analysis of microbial fuel cells based on enriched inoculum from freshwater sediment

  • Research Paper
  • Published:
Bioprocess and Biosystems Engineering Aims and scope Submit manuscript

Abstract

The characterization of anodic microbial communities is of great importance in the study of microbial fuel cells (MFCs). These kinds of devices mainly require a high abundance of anode respiring bacteria (ARB) in the anode chamber for optimal performance. This study evaluated the effect of different enrichments of environmental freshwater sediment samples used as inocula on microbial community structures in MFCs. Two enrichment media were compared: ferric citrate (FeC) enrichment, with the purpose of increasing the ARB percentage, and general enrichment (Gen). The microbial community dynamics were evaluated by polymerase chain reaction followed by denaturing gradient gel electrophoresis (PCR-DGGE) and real time polymerase chain reaction (qPCR). The enrichment effect was visible on the microbial community composition both during precultures and in anode MFCs. Both enrichment approaches affected microbial communities. Shannon diversity as well as β-Proteobacteria and γ-Proteobacteria percentages decreased during the enrichment steps, especially for FeC (p < 0.01). Our data suggest that FeC enrichment excessively reduced the diversity of the anode community, rather than promoting the proliferation of ARB, causing a condition that did not produce advantages in terms of system performance.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Miceli JF, Parameswaran P, Kang DW et al (2012) Enrichment and analysis of anode-respiring bacteria from diverse anaerobic inocula. Environ Sci Technol 46:10349–10355. https://doi.org/10.1021/es301902h

    Article  CAS  PubMed  Google Scholar 

  2. Singh HM, Pathak AK, Chopra K et al (2018) Microbial fuel cells: a sustainable solution for bioelectricity generation and wastewater treatment. Biofuels 7269:1–21. https://doi.org/10.1080/17597269.2017.1413860

    Article  CAS  Google Scholar 

  3. Saratale GD, Saratale RG, Shahid MK et al (2017) A comprehensive overview on electro-active biofilms, role of exo-electrogens and their microbial niches in microbial fuel cells (MFCs). Chemosphere 178:534–547. https://doi.org/10.1016/j.chemosphere.2017.03.066

    Article  CAS  PubMed  Google Scholar 

  4. Aguirre-Sierra A, Bacchetti-De Gregoris T, Berná A et al (2016) Microbial electrochemical systems outperform fixed-bed biofilters in cleaning up urban wastewater. Environ Sci Water Res Technol 2:984–993. https://doi.org/10.1039/C6EW00172F

    Article  CAS  Google Scholar 

  5. Pierra M, Carmona-Martínez AA, Trably E et al (2015) Microbial characterization of anode-respiring bacteria within biofilms developed from cultures previously enriched in dissimilatory metal-reducing bacteria. Biores Technol 195:283–287. https://doi.org/10.1016/j.biortech.2015.07.010

    Article  CAS  Google Scholar 

  6. Doyle LE, Marsili E (2015) Methods for enrichment of novel electrochemically-active microorganisms. Biores Technol 195:273–282. https://doi.org/10.1016/j.biortech.2015.07.025

    Article  CAS  Google Scholar 

  7. Koch C, Harnisch F (2016) Is there a specific ecological niche for electroactive microorganisms? ChemElectroChem 3:1282–1295. https://doi.org/10.1002/celc.201600079

    Article  CAS  Google Scholar 

  8. Zhang YC, Jiang ZH, Liu Y (2015) Application of electrochemically active bacteria as anodic biocatalyst in microbial fuel cells. Chin J Anal Chem 43:155–163. https://doi.org/10.1016/S1872-2040(15)60800-3

    Article  Google Scholar 

  9. Kubota K, Watanabe T, Yamaguchi T, Syutsubo K (2016) Characterization of wastewater treatment by two microbial fuel cells in continuous flow operation. Environ Technol 37:114–120. https://doi.org/10.1080/09593330.2015.1064169

    Article  CAS  PubMed  Google Scholar 

  10. Haavisto JM, Lakaniemi AM, Puhakka JA (2018) Storing of exoelectrogenic anolyte for efficient microbial fuel cell recovery. Environ Technol. https://doi.org/10.1080/09593330.2017.1423395

    Article  PubMed  Google Scholar 

  11. Zhang Y, Zhao Y-G, Guo L, Gao M (2018) Two-stage pretreatment of excess sludge for electricity generation in microbial fuel cell. Environ Technol 1–10. https://doi.org/10.1080/09593330.2017.1422548

  12. Sleutels THJA, Darus L, Hamelers HVM, Buisman CJN (2011) Effect of operational parameters on Coulombic efficiency in bioelectrochemical systems. Biores Technol 102:11172–11176. https://doi.org/10.1016/j.biortech.2011.09.078

    Article  CAS  Google Scholar 

  13. Liu Y, Harnisch F, Fricke K et al (2008) Improvement of the anodic bioelectrocatalytic activity of mixed culture biofilms by a simple consecutive electrochemical selection procedure. Biosens Bioelectron 24:1006–1011. https://doi.org/10.1016/j.bios.2008.08.001

    Article  CAS  Google Scholar 

  14. Kim JR, Min B, Logan BE (2005) Evaluation of procedures to acclimate a microbial fuel cell for electricity production. Appl Microbiol Biotechnol 68:23–30. https://doi.org/10.1007/s00253-004-1845-6

    Article  CAS  PubMed  Google Scholar 

  15. Sathish-Kumar K, Solorza-Feria O, Tapia-Ramírez J et al (2013) Electrochemical and chemical enrichment methods of a sodic–saline inoculum for microbial fuel cells. Int J Hydrog Energy 38:12600–12609. https://doi.org/10.1016/J.IJHYDENE.2012.11.147

    Article  CAS  Google Scholar 

  16. Wang A, Sun D, Ren N et al (2010) A rapid selection strategy for an anodophilic consortium for microbial fuel cells. Biores Technol 101:5733–5735. https://doi.org/10.1016/j.biortech.2010.02.056

    Article  CAS  Google Scholar 

  17. Torres CI, Krajmalnik-Brown R, Parameswaran P et al (2009) Selecting anode-respiring bacteria based on anode potential: phylogenetic, electrochemical, and microscopic characterization. Environ Sci Technol 43:9519–9524. https://doi.org/10.1021/es902165y

    Article  CAS  PubMed  Google Scholar 

  18. Stratford JP, Beecroft NJ, Slade RCT et al (2014) Anodic microbial community diversity as a predictor of the power output of microbial fuel cells. Biores Technol 156:84–91. https://doi.org/10.1016/j.biortech.2014.01.041

    Article  CAS  Google Scholar 

  19. Yamamoto S, Suzuki K, Araki Y et al (2014) Dynamics of different bacterial communities are capable of generating sustainable electricity from microbial fuel cells with organic waste. Microbes Environ 29:145–153. https://doi.org/10.1264/jsme2.ME13140

    Article  PubMed  PubMed Central  Google Scholar 

  20. Agostino V, Ahmed D, Sacco A et al (2017) Electrochemical analysis of microbial fuel cells based on enriched biofilm communities from freshwater sediment. Electrochim Acta 237:133–143. https://doi.org/10.1016/j.electacta.2017.03.186

    Article  CAS  Google Scholar 

  21. Zhi W, Ge Z, He Z, Zhang H (2014) Methods for understanding microbial community structures and functions in microbial fuel cells: a review. Biores Technol 171:461–468. https://doi.org/10.1016/j.biortech.2014.08.096

    Article  CAS  Google Scholar 

  22. Schilirò T, Tommasi T, Armato C et al (2016) The study of electrochemically active planktonic microbes in microbial fuel cells in relation to different carbon-based anode materials. Energy 106:277–284. https://doi.org/10.1016/j.energy.2016.03.004

    Article  CAS  Google Scholar 

  23. Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Webster G, Parkes RJ, Cragg BA et al (2006) Prokaryotic community composition and biogeochemical processes in deep subseafloor sediments from the Peru Margin. FEMS Microbiol Ecol 58:65–85. https://doi.org/10.1111/j.1574-6941.2006.00144.x

    Article  CAS  PubMed  Google Scholar 

  25. O’Sullivan LA, Webster G, Fry JC et al (2008) Modified linker-PCR primers facilitate complete sequencing of DGGE DNA fragments. J Microbiol Methods 75:579–581. https://doi.org/10.1016/j.mimet.2008.08.006

    Article  CAS  PubMed  Google Scholar 

  26. Murri M, Leiva I, Gomez-Zumaquero JM et al (2013) Gut microbiota in children with type 1 diabetes differs from that in healthy children: a case-control study. BMC Med 11:46. https://doi.org/10.1186/1741-7015-11-46

    Article  PubMed  PubMed Central  Google Scholar 

  27. Yang YW, Chen MK, Yang BY et al (2015) Use of 16S rRNA gene-targeted group-specific primers for real-time PCR analysis of predominant bacteria in mouse feces. Appl Environ Microbiol 81:6749–6756. https://doi.org/10.1128/AEM.01906-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Bacchetti De Gregoris T, Aldred N, Clare AS, Burgess JG (2011) Improvement of phylum- and class-specific primers for real-time PCR quantification of bacterial taxa. J Microbiol Methods 86:351–356. https://doi.org/10.1016/j.mimet.2011.06.010

    Article  CAS  Google Scholar 

  29. Hermann-Bank ML, Skovgaard K, Stockmarr A et al (2013) The Gut Microbiotassay: a high-throughput qPCR approach combinable with next generation sequencing to study gut microbial diversity. BMC Genom 14:788. https://doi.org/10.1186/1471-2164-14-788

    Article  CAS  Google Scholar 

  30. Cummings DE, Snoeyenbos-West OL, Newby DT et al (2003) Diversity of Geobacteraceae species inhabiting metal-polluted freshwater lake sediments ascertained by 16S rDNA analyses. Microb Ecol 46:257–269. https://doi.org/10.1007/s00248-002-0005-8

    Article  PubMed  Google Scholar 

  31. de Souza JT, Mazzola M, Raaijmakers JM (2003) Conservation of the response regulator gene gacA in Pseudomonas species. Environ Microbiol 5:1328–1340. https://doi.org/10.1046/j.1462-2920.2003.00438.x

    Article  CAS  PubMed  Google Scholar 

  32. Dridi B, Henry M, El Khéchine A et al (2009) High prevalence of Methanobrevibacter smithii and Methanosphaera stadtmanae detected in the human gut using an improved DNA detection protocol. PLoS One. https://doi.org/10.1371/journal.pone.0007063

    Article  PubMed  PubMed Central  Google Scholar 

  33. Carriço JA, Pinto FR, Simas C et al (2005) Assessment of band-based similarity coefficients for automatic type and subtype classification of microbial isolates analyzed by pulsed-field gel electrophoresis. J Clin Microbiol 43:5483–5490. https://doi.org/10.1128/JCM.43.11.5483-5490.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Cristiani P, Franzetti A, Gandolfi I et al (2013) Bacterial DGGE fingerprints of biofilms on electrodes of membraneless microbial fuel cells. Int Biodeterior Biodegrad 84:211–219. https://doi.org/10.1016/j.ibiod.2012.05.040

    Article  CAS  Google Scholar 

  35. Beecroft NJ, Zhao F, Varcoe JR et al (2012) Dynamic changes in the microbial community composition in microbial fuel cells fed with sucrose. Appl Microbiol Biotechnol 93:423–437. https://doi.org/10.1007/s00253-011-3590-y

    Article  CAS  PubMed  Google Scholar 

  36. Kim JR, Beecroft NJ, Varcoe JR et al (2011) Spatiotemporal development of the bacterial community in a tubular longitudinal microbial fuel cell. Appl Microbiol Biotechnol 90:1179–1191. https://doi.org/10.1007/s00253-011-3181-y

    Article  CAS  PubMed  Google Scholar 

  37. Sun G, Thygesen A, Meyer AS (2015) Acetate is a superior substrate for microbial fuel cell initiation preceding bioethanol effluent utilization. Appl Microbiol Biotechnol 99:4905–4915. https://doi.org/10.1007/s00253-015-6513-5

    Article  CAS  PubMed  Google Scholar 

  38. Sotres A, Díaz-Marcos J, Guivernau M et al (2015) Microbial community dynamics in two-chambered microbial fuel cells: effect of different ion exchange membranes. J Chem Technol Biotechnol 90:1497–1506. https://doi.org/10.1002/jctb.4465

    Article  CAS  Google Scholar 

  39. Stewart EJ (2012) Growing unculturable bacteria. J Bacteriol 194:4151–4160. https://doi.org/10.1128/JB.00345-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Chae KJ, Choi MJ, Lee JW et al (2009) Effect of different substrates on the performance, bacterial diversity, and bacterial viability in microbial fuel cells. Biores Technol 100:3518–3525. https://doi.org/10.1016/j.biortech.2009.02.065

    Article  CAS  Google Scholar 

  41. Liu Q, Yang Y, Mei X et al (2018) Response of the microbial community structure of biofilms to ferric iron in microbial fuel cells. Sci Total Environ 631–632:695–701. https://doi.org/10.1016/j.scitotenv.2018.03.008

    Article  CAS  PubMed  Google Scholar 

  42. Sotres A, Cerrillo M, Viñas M, Bonmatì A (2015) Nitrogen recovery from pig slurry in a two-chambered bioelectrochemical system. Biores Technol 194:373–382. https://doi.org/10.1016/j.biortech.2015.07.036

    Article  CAS  Google Scholar 

  43. Sotres A, Tey L, Bonmatí A, Viñas M (2016) Microbial community dynamics in continuous microbial fuel cells fed with synthetic wastewater and pig slurry. Bioelectrochemistry 111:70–82. https://doi.org/10.1016/j.bioelechem.2016.04.007

    Article  CAS  PubMed  Google Scholar 

  44. Bonmatí A, Sotres A, Mu Y et al (2013) Oxalate degradation in a bioelectrochemical system: Reactor performance and microbial community characterization. Biores Technol 143:147–153. https://doi.org/10.1016/j.biortech.2013.05.116

    Article  CAS  Google Scholar 

  45. Kannaiah Goud R, Venkata Mohan S (2013) Prolonged applied potential to anode facilitate selective enrichment of bio-electrochemically active Proteobacteria for mediating electron transfer: microbial dynamics and bio-catalytic analysis. Biores Technol 137:160–170. https://doi.org/10.1016/j.biortech.2013.03.059

    Article  CAS  Google Scholar 

  46. Hu A, Yang X, Chen N et al (2014) Response of bacterial communities to environmental changes in a mesoscale subtropical watershed, Southeast China. Sci Total Environ 472:746–756. https://doi.org/10.1016/j.scitotenv.2013.11.097

    Article  CAS  PubMed  Google Scholar 

  47. Rago L, Baeza JA, Guisasola A (2016) Increased performance of hydrogen production in microbial electrolysis cells under alkaline conditions. Bioelectrochemistry 109:57–62. https://doi.org/10.1016/j.bioelechem.2016.01.003

    Article  CAS  PubMed  Google Scholar 

  48. Margaria V, Tommasi T, Pentassuglia S et al (2017) Effects of pH variations on anodic marine consortia in a dual chamber microbial fuel cell. Int J Hydrog Energy 42:1820–1829. https://doi.org/10.1016/j.ijhydene.2016.07.250

    Article  CAS  Google Scholar 

  49. Wang Z, Lee T, Lim B et al (2014) Microbial community structures differentiated in a single-chamber air-cathode microbial fuel cell fueled with rice straw hydrolysate. Biotechnol Biofuels 7:9. https://doi.org/10.1186/1754-6834-7-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Rago L, Ruiz Y, Baeza JA et al (2015) Microbial community analysis in a long-term membrane-less microbial electrolysis cell with hydrogen and methane production. Bioelectrochemistry 106:359–368. https://doi.org/10.1016/j.bioelechem.2015.06.003

    Article  CAS  PubMed  Google Scholar 

  51. Lee Y-Y, Kim TG, Cho K (2015) Effects of proton exchange membrane on the performance and microbial community composition of air-cathode microbial fuel cells. J Biotechnol 211:130–137. https://doi.org/10.1016/j.jbiotec.2015.07.018

    Article  CAS  PubMed  Google Scholar 

  52. Spiegelman D, Whissell G, Greer CW (2005) A survey of the methods for the characterization of microbial consortia and communities. Can J Microbiol 51:355–386. https://doi.org/10.1139/w05-003

    Article  CAS  PubMed  Google Scholar 

  53. Rittmann BE, Krajmalnik-Brown R, Halden RU (2008) Pre-genomic, genomic and post-genomic study of microbial communities involved in bioenergy. Nat Rev Microbiol 6:604–612. https://doi.org/10.1038/nrmicro1939

    Article  CAS  PubMed  Google Scholar 

  54. Harnisch F, Rabaey K (2012) The diversity of techniques to study electrochemically active biofilms highlights the need for standardization. ChemSusChem 5:1027–1038. https://doi.org/10.1002/cssc.201100817

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Public Health and Pediatrics, University of Torino, Piazza Polonia 94, 10126, Turin, Italy

    Caterina Armato, Deborah Traversi, Raffaella Degan, Giorgio Gilli & Tiziana Schilirò

  2. Centre for Sustainable Future Technologies (CSFT@PoliTo), Istituto Italiano di Tecnologia, Turin, Italy

    Caterina Armato, Daniyal Ahmed, Valeria Agostino, Valentina Margaria, Adriano Sacco, Marzia Quaglio & Guido Saracco

  3. Department of Applied Science and Technology, Politecnico di Torino, Turin, Italy

    Daniyal Ahmed, Valeria Agostino & Tonia Tommasi

Authors
  1. Caterina Armato
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniyal Ahmed
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Valeria Agostino
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Deborah Traversi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Raffaella Degan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tonia Tommasi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Valentina Margaria
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Adriano Sacco
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Giorgio Gilli
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Marzia Quaglio
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Guido Saracco
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Tiziana Schilirò
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tiziana Schilirò.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher’s Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Armato, C., Ahmed, D., Agostino, V. et al. Anodic microbial community analysis of microbial fuel cells based on enriched inoculum from freshwater sediment. Bioprocess Biosyst Eng 42, 697–709 (2019). https://doi.org/10.1007/s00449-019-02074-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00449-019-02074-0

Keywords

Search

Navigation