Skip to main content
Log in

Identification and topographical characterisation of microbial nanowires in Nostoc punctiforme

  • Short Communication
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Extracellular pili-like structures (PLS) produced by cyanobacteria have been poorly explored. We have done detailed topographical and electrical characterisation of PLS in Nostoc punctiforme PCC 73120 using transmission electron microscopy (TEM) and conductive atomic force microscopy (CAFM). TEM analysis showed that N. punctiforme produces two separate types of PLS differing in their length and diameter. The first type of PLS are 6–7.5 nm in diameter and 0.5–2 µm in length (short/thin PLS) while the second type of PLS are ~20–40 nm in diameter and more than 10 µm long (long/thick PLS). This is the first study to report long/thick PLS in N. punctiforme. Electrical characterisation of these two different PLS by CAFM showed that both are electrically conductive and can act as microbial nanowires. This is the first report to show two distinct PLS and also identifies microbial nanowires in N. punctiforme. This study paves the way for more detailed investigation of N. punctiforme nanowires and their potential role in cell physiology and symbiosis with plants.

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

Access this article

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

References

  • Allen W, Phan G, Waksman G (2012) Pilus biogenesis at the outer membrane of Gram-negative bacterial pathogens. Curr Opin Struct Biol 22:1–7

    Article  Google Scholar 

  • Dodds WK, Gudder DA, Mollenhauer D (1995) The ecology of Nostoc. J Phycol 31:2–18

    Article  CAS  Google Scholar 

  • Duggan PS, Gottardello P, Adams DG (2007) Molecular analysis of genes in Nostoc punctiforme involved in pilus biogenesis and plant infection. J Bacteriol 189:4547–4551

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • El-Naggar MY, Wanger G, Leung KM, Yuzvinsky TD, Southam G, Yang J, Lau WM, Nealson KH, Gorby YA (2010) Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1. Proc Natl Acad Sci USA 107:18127–18131

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Giron JA, Levine MM, Kaper JB (1994) Longus: a long pilus ultrastructure produced by human enterotoxigenic Escherichia coli. Mol Microbiol 12:71–82

    Article  CAS  PubMed  Google Scholar 

  • Gorby YA, Yanina S, McLean JS, Rosso KM, Moyles D, Dohnalkova A, Beveridge TJ, Chang IS, Kim BH, Kim KS, Culley DE, Reed SB, Romine MF, Saffarini DA, Hill EA, Shi L, Elias DA, Kennedy DW, Pinchuk G, Watanabe K, Ishii S, Logan B, Nealson KH, Fredrickson JK (2006) Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc Natl Acad Sci USA 103:11358–11363

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Khayatan B, Meeks JC, Risser DD (2015) Evidence that a modified type IV pilus-like system powers gliding motility and polysaccharide secretion in filamentous cyanobacteria. Mol Microbiol. doi:10.1111/mmi.13205

    PubMed  Google Scholar 

  • Leung KM, Wagner G, Guo Q, Gorby YA, Southam G, Laue WM, Yang J (2011) Bacterial nanowires: conductive as silicon, soft as polymer. Soft Matter 7:6617–6621

    Article  CAS  Google Scholar 

  • Leung KM, Wanger G, El-Naggar MY, Gorby Y, Southam G, Lau WM, Yang J (2013) Shewanella oneidensis MR-1 bacterial nanowires exhibit p-type, tunable electronic behavior. Nano Lett 13:2407–2411

    Article  CAS  PubMed  Google Scholar 

  • Malvankar NS, Vargas M, Nevin KP, Franks AE, Leang C, Kim BC, Inoue K, Mester T, Covalla SF, Johnson JP, Rotello VM, Tuominen MT, Lovley DR (2011) Tunable metallic-like conductivity in microbial nanowire networks. Nat Nanotechnol 6:573–579

    Article  PubMed  Google Scholar 

  • Malvankar NS, Yalcin SE, Tuominen MT, Lovley DR (2014) Visualization of charge propagation along individual pili proteins using ambient electrostatic force microscopy. Nat Nanotechnol 9:1012–1017

    Article  CAS  PubMed  Google Scholar 

  • Meeks JC (1998) Symbiosis between nitrogen-fixing cyanobacteria and plants. Biosciences 48:266–276

    Article  Google Scholar 

  • Meeks JC (2006) Molecular mechanisms in the nitrogen-fixing Nostoc-bryophyte symbiosis. Prog Mol Subcell Biol 41:165–196

    Article  CAS  PubMed  Google Scholar 

  • Meeks JC, Elhai J, Thiel T, Potts M, Larimer F, Lamerdin J, Predki P, Atlas R (2001) An overview of the genome of Nostoc punctiforme, a multicellular, symbiotic cyanobacterium. Photosynth Res 70:85–106

    Article  CAS  PubMed  Google Scholar 

  • Morita M, Malvankar NS, Franks AE, Summers ZM, Giloteaux L, Rotaru AE, Rotaru C, Lovley DR (2011) Potential for direct interspecies electron transfer in methanogenic wastewater digester aggregates. MBio 2:e00159-11

    Article  PubMed Central  PubMed  Google Scholar 

  • Nakasugi K, Neilan BA (2005) Identification of pilus-like structures and genes in Microcystis aeruginosa PCC7806. Appl Environ Microbiol 71:7621–7625

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pelicic V (2008) Type IV pili: e pluribus unum? Mol Microbiol 68:827–837

    Article  CAS  PubMed  Google Scholar 

  • Pisciotta JM, Zou Y, Baskakov IV (2010) Light-dependent electrogenic activity of cyanobacteria. PLoS ONE 5:e10821

    Article  PubMed Central  PubMed  Google Scholar 

  • Reguera G (2011) When microbial conversations get physical. Trends Microbiol 19:105–113

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR (2005) Extracellular electron transfer via microbial nanowires. Nature 435:1098–1101

    Article  CAS  PubMed  Google Scholar 

  • Rotaru AE, Shrestha PM, Liu F, Shrestha M, Shrestha D, Embree M, Zengler K, Wardman C, Nevin KP, Lovley DR (2014) A new model for electron flow during anaerobic digestion: direct interspecies electron transfer to Methanosaeta for the reduction of carbon dioxide to methane. Energy Environ Sci 7:408–415

    Article  CAS  Google Scholar 

  • Summers ZM, Fogarty HE, Leang C, Franks AE, Malvankar NS, Lovley DR (2010) Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria. Science 330:1413–1415

    Article  CAS  PubMed  Google Scholar 

  • Sure S, Torriero AA, Gaur A, Li LH, Chen Y, Tripathi C, Adholeya A, Ackland ML, Kochar M (2015) Inquisition of Microcystis aeruginosa and Synechocystis nanowires: characterization and modelling. Antonie Van Leeuwenhoek 108:1213–1225

    Article  CAS  PubMed  Google Scholar 

  • Vaara T, Vaara M (1988) Cyanobacterial fimbriae. Methods Enzymol 167:189–195

    Article  Google Scholar 

  • Vargas M, Malvankar NS, Tremblay PL, Leang C, Smith JA, Patel P, Synoeyenbos-West O, Nevin KP, Lovley DR (2013) Aromatic amino acids required for pili conductivity and long-range extracellular electron transport in Geobacter sulfurreducens. MBio 4:e00105-13

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank The Energy and Resources Institute, India and Deakin University, Australia for providing financial support and required infrastructure to carry out the research work. SS was supported by Deakin University HDR scholarship (Candidate ID—212082401).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mandira Kochar.

Ethics declarations

Conflict of Interest

None.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1951 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sure, S., Torriero, A.A.J., Gaur, A. et al. Identification and topographical characterisation of microbial nanowires in Nostoc punctiforme . Antonie van Leeuwenhoek 109, 475–480 (2016). https://doi.org/10.1007/s10482-015-0644-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-015-0644-7

Keywords

Navigation