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

Applied Microbiology and Biotechnology

Volumn 98, Issue 21, 2014, Pages 9021-9031

  Sivakumar, Krishnakumar ^a,b   Wang, Victor Bochuan ^a,d   Chen, Xiaofen ^g   Bazan, Guillermo C ^g   Kjelleberg, Staffan ^a,e,f   Loo, Say Chye Joachim ^a,d   Cao, Bin ^a,c  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^e NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^f UNIVERSITY OF NEW SOUTH WALES   (Australia)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Biofilm; Conjugated oligoelectrolyte; DSSN+; Shewanella oneidensis

Indexed keywords

BACTERIA; BIOACTIVITY; BIOFILMS; CELLS; CYTOLOGY; ELECTROPHYSIOLOGY; ENZYMES;

BIOELECTROCHEMICAL DEVICES; CONJUGATED OLIGOELECTROLYTE; CONJUGATED OLIGOELECTROLYTES; DSSN; EXTRACELLULAR CONCENTRATION; EXTRACELLULAR ENZYME ACTIVITY; MEMBRANE PERMEABILIZATION; SHEWANELLA ONEIDENSIS;

MEMBRANES;

ENZYME; FERRIC HYDROXIDE; FERRIC ION; STILBENE DERIVATIVE;

CELL MEMBRANE; CELL SURVIVAL; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OXIDATION REDUCTION REACTION; PERMEABILITY; SHEWANELLA;

CELL MEMBRANE; CELL SURVIVAL; ENZYMES; FERRIC COMPOUNDS; OXIDATION-REDUCTION; PERMEABILITY; SHEWANELLA; STILBENES;

EID: 84920255007     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-5973-3     Document Type: Article

References (54)

1. Alcalde M, Ferrer M, Plou FJ (2007) Environmental biocatalysis: from remediation with enzymes to novel green processes. Biocatal Biotransform 25(2–4):113–113
2. Belchik SM, Kennedy DW, Dohnalkova AC, Wang Y, Sevinc PC, Wu H, Lin Y, Lu HP, Fredrickson JK, Shi L (2011) Extracellular reduction of hexavalent chromium by cytochromes MtrC and OmcA of Shewanella oneidensis MR-1. Appl Environ Microbiol 77(12):4035–41
3. Beuling E, Van Dusschoten D, Lens P, Van Den Heuvel J, Van As H, Ottengraf S (1998) Characterization of the diffusive properties of biofilms using pulsed field gradient-nuclear magnetic resonance. Biotechnol Bioeng 60(3):283–291
4. Branda SS, Vik Å, Friedman L, Kolter R (2005) Biofilms: the matrix revisited. Trends Microbiol 13(1):20–26
5. Bretschger O, Obraztsova A, Sturm CA, Chang IS, Gorby YA, Reed SB, Culley DE, Reardon CL, Barua S, Romine MF (2007) Current production and metal oxide reduction by Shewanella oneidensis MR-1 wild type and mutants. Appl Environ Microbiol 73(21):7003–7012
6. Cao B, Ahmed B, Kennedy DW, Wang Z, Shi L, Marshall MJ, Fredrickson JK, Isern NG, Majors PD, Beyenal H (2011) Contribution of extracellular polymeric substances from Shewanella sp. HRCR-1 biofilms to U(VI) immobilization. Environ Sci Technol 45(13):5483–90
7. Chen C-Y, Nace G, Irwin P (2003) A 6×6 drop plate method for simultaneous colony counting and MPN enumeration of Campylobacter jejuni, Listeria monocytogenes, and Escherichia coli. J Microbiol Methods 55:475–479
8. Chen JJ, Chen W, He H, Li DB, Li WW, Xiong L, Yu HQ (2013) Manipulation of microbial extracellular electron transfer by changing molecular structure of phenazine-type redox mediators. Environ Sci Technol 47(2):1033–1039
9. Clark ME, He Z, Redding AM, Joachimiak MP, Keasling JD, Zhou J, Arkin AP, Mukhopadhyay A, Fields MW (2012) Transcriptomic and proteomic analyses of Desulfovibrio vulgaris biofilms: Carbon and energy flow contribute to the distinct biofilm growth state. BMC Genomics 13(1):138
10. Coursolle D, Gralnick JA (2012) Reconstruction of extracellular respiratory pathways for iron (III) reduction in Shewanella oneidensis strain MR-1. Front Microbiol 3:56
11. Coursolle D, Baron DB, Bond DR, Gralnick JA (2010) The Mtr respiratory pathway is essential for reducing flavins and electrodes in Shewanella oneidensis. J Bacteriol 192(2):467–474
12. Covington ED, Gelbmann CB, Kotloski NJ, Gralnick JA (2010) An essential role for UshA in processing of extracellular flavin electron shuttles by Shewanella oneidensis. Mol Microbiol 78(2):519–532
13. Du J, Thomas AW, Chen XF, Garner LE, Vandenberg CA, Bazan GC (2013) Increased ion conductance across mammalian membranes modified with conjugated oligoelectrolytes. Chem Commun 49(83):9624–9626
14. Flemming H-C, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8(9):623–633
15. Fredrickson JK, Zachara JM (2008) Electron transfer at the microbe-mineral interface: a grand challenge in biogeochemistry. Geobiology 6(3):245–253
16. Fredrickson JK, Romine MF, Beliaev AS, Auchtung JM, Driscoll ME, Gardner TS, Nealson KH, Osterman AL, Pinchuk G, Reed JL, Rodionov DA, Rodrigues JLM, Saffarini DA, Serres MH, Spormann AM, Zhulin IB, Tiedje JM (2008) Towards environmental systems biology of Shewanella. Nat Rev Microbiol 6(8):592–603
17. Garner LE, Park J, Dyar SM, Chworos A, Sumner JJ, Bazan GC (2010) Modification of the optoelectronic properties of membranes via insertion of amphiphilic phenylenevinylene oligoelectrolytes. J Am Chem Soc 132(29):10042–10052
18. Garner LE, Thomas AW, Sumner JJ, Harvey SP, Bazan GC (2012) Conjugated oligoelectrolytes increase current response and organic contaminant removal in wastewater microbial fuel cells. Energ Environ Sci 5(11):9449–9452
19. Gross R, Hauer B, Otto K, Schmid A (2007) Microbial biofilms: new catalysts for maximizing productivity of long–term biotransformations. Biotechnol Bioeng 98(6):1123–1134
20. Halan B, Buehler K, Schmid A (2012) Biofilms as living catalysts in continuous chemical syntheses. Trends Biotechnol 30(9):453–465
21. Hartmann M, Jung D (2010) Biocatalysis with enzymes immobilized on mesoporous hosts: the status quo and future trends. J Mater Chem 20(5):844–857
22. Hinks J, Wang Y, Poh WH, Donose BC, Thomas AW, Wuertz S, Loo SC, Bazan GC, Kjelleberg SL, Mu Y, Seviour TW (2014) Modeling the membrane insertion of molecules designed for transmembrane electron transfer. Langmuir 30(9):2429–2440
23. Hou H, Chen X, Thomas AW, Catania C, Kirchhofer ND, Garner LE, Han A, Bazan GC (2013) Conjugated oligoelectrolytes increase power generation in E. coli microbial fuel cells. Adv Mater 25(11):1593–1597
24. Kiely PD, Regan JM, Logan BE (2011) The electric picnic: synergistic requirements for exoelectrogenic microbial communities. Curr Opin Biotechnol 22(3):378–385
25. Kotloski NJ, Gralnick JA (2013) Flavin electron shuttles dominate extracellular electron transfer by Shewanella oneidensis. mBio 4(1):e00553–12
26. Leon R, Fernandes P, Pinheiro H, Cabral J (1998) Whole-cell biocatalysis in organic media. Enzyme Microb Technol 23(7):483–500
27. Leresche JE, Meyer H-P (2006) Chemocatalysis and biocatalysis (biotransformation): some thoughts of a chemist and of a biotechnologist. Org Proc Res Develop 10(3):572–580
28. Lewandowski Z, Beyenal H (2007) Fundamentals of biofilm research. CRC Press
29. Lies DP, Hernandez ME, Kappler A, Mielke RE, Gralnick JA, Newman DK (2005) Shewanella oneidensis MR-1 uses overlapping pathways for iron reduction at a distance and by direct contact under conditions relevant for biofilms. Appl Environ Microbiol 71(8):4414–4426
30. Liu XW, Sun XF, Chen JJ, Huang YX, Xie JF, Li WW, Sheng GP, Zhang YY, Zhao F, Lu R, Yu HQ (2013) Phenothiazine derivative-accelerated microbial extracellular electron transfer in bioelectrochemical system. Sci Rep 3:1616
31. Marshall MJ, Beliaev AS, Dohnalkova AC, Kennedy DW, Shi L, Wang Z, Boyanov MI, Lai B, Kemner KM, McLean JS, Reed SB, Culley DE, Bailey VL, Simonson CJ, Saffarini DA, Romine MF, Zachara JM, Fredrickson JK (2006) c-Type cytochrome-dependent formation of U(IV) nanoparticles by Shewanella oneidensis. PLoS Biol 4(9):e268
32. Marshall MJ, Plymale AE, Kennedy DW, Shi L, Wang Z, Reed SB, Dohnalkova AC, Simonson CJ, Liu C, Saffarini DA (2008) Hydrogenase–and outer membrane c–type cytochrome–facilitated reduction of technetium (VII) by Shewanella oneidensis MR–1. Environ Microbiol 10(1):125–136
33. Marsili E, Baron DB, Shikhare ID, Coursolle D, Gralnick JA, Bond DR (2008) Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci U S A 105(10):3968–3973
34. Mohanty A, Kathawala MH, Zhang J, Chen WN, Loo JSC, Kjelleberg S, Yang L, Cao B (2013) Biogenic tellurium nanorods as a novel antivirulence agent inhibiting pyoverdine production in Pseudomonas aeruginosa. Biotechnol Bioeng 111(5):858–865
35. Myers CR, Nealson KH (1988) Microbial reduction of manganese oxides: Interactions with iron and sulfur. Geochim Cosmochim Act 52(11):2727–2732
36. Nikolova P, Ward OP (1993) Whole cell biocatalysis in nonconventional media. J Ind Microbiol 12(2):76–86
37. Polizzi KM, Bommarius AS, Broering JM, Chaparro-Riggers JF (2007) Stability of biocatalysts. Curr Opin Chem Biol 11(2):220–225
38. Renslow RS, Majors PD, McLean JS, Fredrickson JK, Ahmed B, Beyenal H (2010) In situ effective diffusion coefficient profiles in live biofilms using pulsed–field gradient nuclear magnetic resonance. Biotechnol Bioeng 106(6):928–937
39. Richardson DJ, Butt JN, Fredrickson JK, Zachara JM, Shi L, Edwards MJ, White G, Baiden N, Gates AJ, Marritt SJ (2012) The ‘porin–cytochrome’model for microbe–to–mineral electron transfer. Mol Microbiol 85(2):201–212
40. Rosche B, Li XZ, Hauer B, Schmid A, Buehler K (2009) Microbial biofilms: a concept for industrial catalysis? Trends Biotechnol 27(11):636–643
41. Santacoloma PA, Gr S, Gernaey KV, Woodley JM (2010) Multienzyme-catalyzed processes: next-generation biocatalysis. Org Proc Res Develop 15(1):203–212
42. Shi L, Richardson DJ, Wang Z, Kerisit SN, Rosso KM, Zachara JM, Fredrickson JK (2009) The roles of outer membrane cytochromes of Shewanella and Geobacter in extracellular electron transfer. Environ Microbiol Rep 1(4):220–227
43. Simonides W, Zaremba R, Van Hardeveld C, Van der Laarse W (1988) A nonenzymatic method for the determination of picomole amounts of lactate using HPLC: its application to single muscle fibers. Anal Biochem 169(2):268–273
44. Singh R, Paul D, Jain RK (2006) Biofilms: Implications in bioremediation. Trends Microbiol 14(9):389–397
45. Stewart PS (2003) Diffusion in biofilms. J Bacteriol 185(5):1485–1491
46. Thormann KM, Saville RM, Shukla S, Pelletier DA, Spormann AM (2004) Initial phases of biofilm formation in Shewanella oneidensis MR-1. J Bacteriol 186(23):8096–8104
47. Tsoligkas AN, Winn M, Bowen J, Overton TW, Simmons MJH, Goss RJM (2011) Engineering biofilms for biocatalysis. ChemBioChem 12(9):1391–1395
48. Wang Z, Liu C, Wang X, Marshall MJ, Zachara JM, Rosso KM, Dupuis M, Fredrickson JK, Heald S, Shi L (2008) Kinetics of reduction of Fe (III) complexes by outer membrane cytochromes MtrC and OmcA of Shewanella oneidensis MR-1. Appl Environ Microbiol 74(21):6746–6755
49. Wang VB, Du J, Chen X, Thomas AW, Kirchhofer ND, Garner LE, Maw MT, Poh WH, Hinks J, Wuertz S, Kjellenberg S, Zhang Q, Loo JS, Bazan GC (2013) Improving charge collection in Escherichia coli–carbon electrode devices with conjugated oligoelectrolytes. Phys Chem Chem Phys 15(16):5867–5872
50. Wang VB, Kirchhofer ND, Chen X, Tan MYL, Sivakumar K, Cao B, Zhang Q, Kjelleberg S, Bazan GC, Loo JSC, Marsili E (2014) Comparison of flavins and a conjugated oligoelectrolyte in stimulating extracellular electron transport from Shewanella oneidensis MR-1. Electrochem Commun 41:55–58
51. Wu C, Cheng YY, Li BB, Li WW, Li DB, Yu HQ (2013) Electron acceptor dependence of electron shuttle secretion and extracellular electron transfer by Shewanella oneidensis MR-1. Bioresource Technol 136:711–714
52. Yong YC, Yu YY, Yang Y, Liu J, Wang JY, Song H (2013) Enhancement of extracellular electron transfer and bioelectricity output by synthetic porin. Biotechnol Bioeng 110(2):408–416
53. Yu YY, Chen HL, Yong YC, Kim DH, Song H (2011) Conductive artificial biofilm dramatically enhances bioelectricity production in Shewanella-inoculated microbial fuel cells. Chem Commun 47(48):12825–12827
54. Zhang Y, Ng CK, Cohen Y, Cao B (2014) Cell growth and protein expression of Shewanella oneidensis in biofilms and hydrogel-entrapped cultures. Mol BioSys 10(5):1035–1042