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Applied Microbiology and Biotechnology

, Volume 98, Issue 21, pp 9021–9031 | Cite as

Membrane permeabilization underlies the enhancement of extracellular bioactivity in Shewanella oneidensis by a membrane-spanning conjugated oligoelectrolyte

  • Krishnakumar Sivakumar
  • Victor Bochuan Wang
  • Xiaofen Chen
  • Guillermo C. Bazan
  • Staffan Kjelleberg
  • Say Chye Joachim Loo
  • Bin Cao
Applied microbial and cell physiology

Abstract

A stilbene-based membrane spanning conjugated oligoelectrolyte 4,4′-bis(4′-N,N-bis(6″-(N,N,N-trimethyl ammonium) hexyl) amino)-styryl) stilbene tetraiodide (DSSN+) has been reported to be able to interact with bacterial cells and enhance their bioelectricity generation in bioelectrochemical devices, although the mechanism remains elusive. The goal of this study was to elucidate the impacts of DSSN+ on extracellular bioactivity and the underlying mechanism. Specifically, extracellular ferrihydrite reduction by Shewanella oneidensis was used to evaluate the influence of cell-DSSN+ interaction. Our results show that DSSN+ enhanced ferrihydrite reduction by S. oneidensis in a growth-dependent manner. The incorporation of DSSN+ into S. oneidensis cell membrane increased the extracellular concentration of redox shuttles, i.e., flavins, and extracellular enzyme activities without significantly decreasing cell viability. The findings suggested that membrane permeabilization is the dominant mechanism for the enhancement of extracellular bioactivity in S. oneidensis by DSSN+. We further demonstrated that the interaction between DSSN+ and S. oneidensis cells enhanced biofilm formation and stability without compromising the overall biofilm activity. Taken together, our results suggest that membrane spanning conjugated oligoelectrolytes, of which DSSN+ is one of many possible molecular structures, may be applied to enhance extracellular bioactivity in bacteria toward more efficient biofilm-based biocatalysis.

Keywords

Biofilm Conjugated oligoelectrolyte Shewanella oneidensis DSSN+ 

Notes

Acknowledgments

We thank Anee Mohanty, Weijie Liu, and Manisha Mukherjee for their assistance in RNA extraction and qPCR; Chun Kiat Ng and Yuanzhao Ding for flow cell biofilms and CLSM image analyses. We also thank Stefan Wuertz and Liang Yang for their useful discussion and advices. This research was supported by the National Research Foundation and Ministry of Education Singapore under its Research Centre of Excellence Programme, Singapore Centre on Environmental Life Sciences Engineering (SCELSE) (M433C70000.M4220001.C70) and M4330005.C70) and a Start-up Grant (M4080847.030) from College of Engineering, Nanyang Technological University, Singapore. The work at UCSB was supported by the Institute for Collaborative Biotechnologies through grant W911NF-09-0001 from the U.S. Army Research Office. The content of the information does not necessarily reflect the position or the policy of the US Government, and no official endorsement should be inferred.

Supplementary material

253_2014_5973_MOESM1_ESM.pdf (81 kb)
ESM 1 (PDF 80 kb)

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Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Krishnakumar Sivakumar
    • 1
    • 2
  • Victor Bochuan Wang
    • 1
    • 4
  • Xiaofen Chen
    • 7
  • Guillermo C. Bazan
    • 7
  • Staffan Kjelleberg
    • 1
    • 5
    • 6
  • Say Chye Joachim Loo
    • 1
    • 4
  • Bin Cao
    • 1
    • 3
  1. 1.Singapore Centre on Environmental Life Sciences EngineeringNanyang Technological UniversitySingaporeSingapore
  2. 2.Interdisciplinary Graduate SchoolNanyang Technological UniversitySingaporeSingapore
  3. 3.School of Civil and Environmental EngineeringNanyang Technological UniversitySingaporeSingapore
  4. 4.School of Materials Science and EngineeringNanyang Technological UniversitySingaporeSingapore
  5. 5.School of Biological SciencesNanyang Technological UniversitySingaporeSingapore
  6. 6.School of Biotechnology and Biomolecular SciencesThe University of New South WalesSydneyAustralia
  7. 7.Department of Materials and Chemistry & BiochemistryUniversity of CaliforniaSanta BarbaraUSA

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