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Erable, Benjamin and Bergel, Alain ( 2009) First
air-tolerant effective stainless steel microbial anode obtained from a natural
marine biofilm. Bioresource Technology, vol. 100 (n°13). pp. 3302-3307.
ISSN 0960-8524
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First air-tolerant effective stainless steel microbial anode obtained
from a natural marine biofilm
Benjamin Erable
*, Alain Bergel
Laboratoire de Génie Chimique, CNRS, Université de Toulouse, 5 rue Paulin Talabot, BP 1301, 31106 Toulouse, France
Keywords:
Electrochemically active biofilm Marine biofilm
Stainless steel Microbial fuel cell Bioanode
a b s t r a c t
Microbial anodes were constructed with stainless steel electrodes under constant polarisation. The sea-water medium was inoculated with a natural biofilm scraped from harbour equipment. This procedure led to efficient microbial anodes providing up to 4 A/m2
for 10 mM acetate oxidation at 0.1 V/SCE. The whole current was due to the presence of biofilm on the electrode surface, without any significant involvement of the abiotic oxidation of sulphide or soluble metabolites. Using a natural biofilm as inoc-ulum ensured almost optimal performance of the biofilm anode as soon as it was set up; the procedure also proved able to form biofilms in fully aerated media, which provided up to 0.7 A/m2. The current den-sity was finally raised to 8.2 A per square meter projected surface area using a stainless steel grid. The inoculating procedure used here combined with the control of the potential revealed, for the first time, stainless steel as a very competitive material for forming bioanodes with natural microbial consortia.
1. Introduction
Marine sediments are rich in organic compounds that are con-verted by indigenous microorganisms into fermentation products, the best known being acetate. Benthic microbial fuel cells (MFCs) can supply electrical energy directly from the oxidation of these fermentation products into CO2. Reimers and Tender were the first to present this concept with a graphite anode buried in marine sediments connected to a cathode immersed in oxygenated seawa-ter (Reimers et al., 2001; Tender et al., 2002). Microorganisms that adhered to the anode were shown to be able to catalyse the oxida-tion of acetate and other compounds, transferring the electrons produced directly to the anode. These early works gave current densities of the order of 100 mA/m2. Using a modified graphite an-ode with electronic mediators (AQDS, Mn2+, Ni2+) improved the performance of microbial anodes up to 550 mA/m2(Lowy et al.,
2006). Current density has also been enhanced by addition of sub-strates such as cysteine, chitin or cellulose into the sediments ( Lo-gan et al., 2005; Farzaneh et al., 2007).
At the same time, several bacteria or media have been studied under constant potential chronoamperometry (CA) to focus on the anode process only (Cho and Ellington, 2007; Parot et al., 2008a,b). In this way, pure cultures of microorganisms from mar-ine environments such as Geobacter sulfurreducens (Bond et al., 2002; Gregory et al., 2004; Dumas et al., 2008a,b), Desulfuromonas acetoxidans (Bond et al., 2002;Bond and Lovley, 2003),
Desulfobul-bus propionicus (Holmes et al., 2004) have been used to form bioa-nodes and have generally led to higher values of current densities, for example up to 8.0 A/m2 with a biofilm of G. sulfurreducens developed on a graphite anode polarised at +0.2 V/Ag–AgCl ( Du-mas et al., 2008a).
Graphite is commonly used in different forms as an anode material (Logan et al., 2007). A few studies have been aimed at developing stainless steel anodes, because of the better expected mechanical properties of stainless steels for long-term operations and large-scale extrapolation into easy-to-handle equipment.
Stainless steel anodes implemented in benthic MFCs have re-vealed a complex behaviour (Dumas et al., 2007) that may be partly controlled by electrochemical and semi-conductive proper-ties of the surface oxide layers (Dumas et al., 2008c). Nevertheless, keeping stainless steel anodes in well-controlled laboratory condi-tions (constant potential chronoamperometry), with a G. sulfurre-ducens biofilm has led to current density of up to 2.4 A/m2 for acetate oxidation (Dumas et al., 2008b).
We have recently proposed a new procedure for constructing electrochemically active (EA) biofilms, which consisted of using natural biofilms as inoculum rather than samples collected from bulk sediments as is commonly the case. Natural biofilms were scraped from a sea environment and used as inoculum to construct EA biofilms on graphite anodes under constant polarisation. Fol-lowing this procedure, microbial graphite anodes led to signifi-cantly higher current densities, up to 7.9 A/m2for the oxidation of acetate at 100 mV vs. SCE (Erable et al., in press). The purpose of the present work was to check the capacity of stainless steel to form efficient microbial anodes with microbial consortia coming
* Corresponding author.
from marine environments. In order to use the best possible conditions, the microbial anodes were constructed under constant polarisation and natural marine biofilms were used as inoculum. 2. Experimental
2.1. Marine biofilm
Natural marine biofilm was collected from a plastic floating bridge in the port of La Tremblade (Atlantic Ocean, France). The floating bridge is situated in the low water zone and is conse-quently in direct contact with sediment for 6 h a day. The biofilm was harvested using a plastic scraper and around 50 ml of bioma-terial was stored in a glass bottle with 20 ml of fresh seawater for three days at ambient temperature. The seawater used for the experiments was from the same location.
2.2. Electrochemical instrumentation and set-up
Experiments were performed at constant potential polarisation (chronoamperometry) using a conventional three-electrode sys-tem implemented with a multi-potentiostat (VMP2 Bio-Logic SA, software EC-Lab v.8.3, Bio-Logic SA). Experiments were carried out in 500 ml reactors containing 250 ml of seawater supple-mented with acetate (10 mM final concentration) and inoculated with 250 ml of marine biofilm samples. Reactors were closed her-metically, with no gas flow. Stainless steel 254SMO (Fe 56.1%, Cr 19.9%, Ni 17.8%, Mo 6%, N 0.2%) plates of 25 cm2projected surface area were used as working electrodes. The stainless steel was cleaned before each experiment by immersion in 2% HF/0.5 M HNO3 solution for 20 min and was rinsed for 1 h with distilled water. The working electrodes were embedded vertically down to the bottom of the reactor and the electric contact was made with a titanium wire. The auxiliary electrode was a 20 cm2 pro-jected surface area platinum mesh and was maintained near to the surface layer of the medium. All electric potentials were re-ported against a Saturated Calomel standard reference Electrode (SCE, Radiometer Analytical, TR100) protected with a second por-ous frit. The potential of the working electrode was fixed at 100 mV/SCE during chronoamperometry. Cyclic voltammetry was performed in situ on the active anodes and on control elec-trodes that were in the same reactor but not polarised. The poten-tial was scanned 3 times between 700 and 300 mV/SCE at scan rate of 10 mV s1and only the last scan was reported in this study. 2.3. Microscopy
The microbial colonisation of the stainless steel coupons was imaged at the end of the experiments by epifluorescence micros-copy. Stainless steel samples were washed carefully with seawater to remove all materials except attached biofilms. The biofilm was stained with 0.03% orange acridine (A6014, Sigma) for 10 min. The samples were left to dry in ambient air and analysed with a Carl Zeiss Axiotech 100 microscope equipped for epifluorescence with an HBO 50/ac mercury light source and the Zeiss 09 filter (excitor HP450-490, reflector FT 10, barrier filter LP520). Images were acquired with a monochrome digital camera (Evolution VF) and treated with the Image-Pro Plus 5.0 software to recompose 3-D images.
3. Results and discussion
A 25 cm2stainless steel working electrode was maintained at 100 mV/SCE in a reactor inoculated with a natural marine biofilm scratched from a plastic floating bridge. Using natural biofilms has
been demonstrated to promote electrode colonisation by electro-chemically active microorganisms (Ryckelynck et al., 2005; Rei-mers et al., 2001, 2006). After 2 days, a current density was detected, which increased continuously to reach 4.0 A/m2 after 12 days (Fig. 1A). The mechanism of microbial electrocatalysis in anoxic sediments has been widely investigated. It has been estab-lished that the current provided by graphite anodes embedded in sediments is due to the direct transfer of the electrons coming from the microbial metabolism of acetate on the one hand, combined with the abiotic oxidation of S2accumulated in the sediments on the other hand (Lowy et al., 2006; Reimers et al., 2006; Tender et al., 2007). In order to assess the part of current that might be due to the possible abiotic oxidation of S2or other secondary meta-bolic compounds that may have accumulated in the medium, a clean stainless steel electrode was immerged in the medium at day 12. In parallel, the biofilm-coated anode was plunged into a new reactor containing 500 ml of fresh seawater with 10 mM ace-tate. Both electrodes were polarised at 100 mV and the current was followed on each anode for a week (Fig. 1B and C). The current density remained at almost the same value with the biofilm-anode in the fresh medium for around 3 days and then started to increase again. In contrast, no current was observed on the clean electrode plunged in the environment which had been already used for 12 days. Consequently, in this case, no abiotic reaction was in-volved in the production of current and the biofilm was responsi-ble for the whole current observed under constant potential polarisation. In contrast to what has been observed with graphite anodes in sediments, no compound that may have accumulated in the medium was involved in the production of current here.
Cyclic voltammetry (CV) performed at day 12 (Fig. 2) with the biofilm-coated anode firstly in the initial medium and then with the same electrode immerged in fresh seawater confirmed only a slight decrease of current in fresh seawater, as observed under chronoamperometry. Most of the current was consequently due to the presence of the biofilm. The slight decrease was certainly due to the effect on biofilm activity of the modification of environ-mental parameters (oxygen presence, pH, substrate concentration) when the medium was changed because of the low biofilm thick-ness (50–60
lm). At day 12 a clean electrode was plunged into
the reactor containing the initial medium. CV performed with this clean electrode showed a weak oxidation reaction from around 0.3 V with a plateau reaching 0.4 A/m2at 0.1 V, while no cur-rent (less than 0.05 A/m2) was detected under chronoamperometry (less than 0.05 A/m2). Such a discrepancy between the behaviour observed by CV and CA has already been noted with metallic an-odes (Dumas et al., 2008b): a significant current is detected by CV before the chronoamperometry starts to provide current. This difference has been attributed to the beginning of the settlement0 0.5 1 1.5 2 2.5 3 3.5 4 4.5 5 0 5 10 15 20 Time - Days C u rr en t d en si ty - A /m 2 (A) (B) (C)
Fig. 1. Microbial current production with a working stainless steel electrode polarised at 100 mV vs. SCE. (A) Initial. (B) In a new fresh medium. (C) With a clean electrode plunged into the reactor at day 12.
of EA microbial cells (Parot et al., 2008b). The first settled cells are assumed to be able to implement fast reversible electron exchange with the electrode. Only a part of the redox chain of the cells is in-volved in the oxidation/reduction process, which does not reach the metabolism of acetate oxidation. This process is thus similar to a redox charge/discharge of the internal electron transfer system of the cells, it and can be detected by CV but cannot sustain station-ary current under CA. Moreover this process was certainly respon-sible for the large ‘‘charge/discharge” current that enlarged the CV curves. The hysteresis phenomenon cannot be attributed here to pure capacitive current because it was not observed with the clean electrode. It was directly linked to the presence of the EA biofilm on the electrode surface. By the way, such behaviour was not
reproducible, and in some experiments the hysteresis effect almost disappeared (e.g., as inFig. 5) indicating that the settlement of the first EA microbial cells was not fully mastered.
Biofilms were observed by epifluorescence microscopy at the end of the experiments (day 18). The numerical 3-D biofilm recon-struction showed a homogeneous distribution of biofilm on the stainless steel surface (Fig. 3) with a coverage ratio of around 90% and a biofilm thickness evaluated at 80–90
lm. The biofilm
seemed to be supported by some kind of pillars that anchored the biofilm and supported it a few tens of micrometres above the electrode surface. This morphology was not due to the roughness of the stainless steel surface, which was only around 0.3lm (
Du-mas et al., 2008b; Erable et al., in press) and consequently could not explain the height of the pillars that formed the lower layer of the biofilm. This kind of structure can be compared to the well known mushroom configuration that has been evidenced and widely studied with pure cultures of Pseudomonas aeruginosa (Takenaka et al., 2001). Biofilms formed in close to quiescent hydrodynamic conditions are known to present a high degree of void and marked channels in their internal structure. Here the 3-D pictures revealed a similar but exacerbated structure, where anchoring to the surface seemed to be minimal. It can be supposed that the microbial cells in contact with the electrode surface, which form the ‘‘pillars” of the structure here, play a key role in the elec-tron transfer pathway. This physical observation reinforced the model that was suggested previously from electrochemical investi-gations, which assumed the specific role of an ‘‘electrochemical gate” for the microbial cells that settled on the electrode surface first (Dumas et al., 2008b; Parot et al., 2008a).The concentration of dissolved oxygen present in the aqueous phase is known to influence the structure and permeability of bio-films (Jin et al., 2006). The mechanical biofilm resistance in the presence of high concentrations of dissolved oxygen is lower to that in an anoxic environment. This has been attributed to rela-tively higher biofilm porosity and smaller amounts of exopolymer-ic substances (EPS) in biofilms growing with oxygen (Kim et al., 2006). In MFC, the presence of oxygen in the anodic side is often a source of problems and leads to the fall-off in the power gener-ated (Ryckelynck et al., 2005; Dulon et al., 2006; Reimers et al., 2006). Depending on the potential of the anode and its electro-kinetic properties, dissolved oxygen may reduce directly on the an-ode and consequently lower the current provided to the external circuit. On the other hand, oxygen may be used by the microbial cells as an electron acceptor, diverting a part of the electron flow from the anode. Oxygen can also cause inactivation of the cells, as reported byKim et al. (1999)who observed that the electroac-tivity of a pure culture of Shewanella putrefaciens IR-1 was inacti-vated reversibly by exposure to air.
The sensitivity of our biofilms to oxygen was checked by form-ing two EA-biofilms in parallel in two electrochemical reactors
-8 -6 -4 -2 0 2 4 6 8 10 12 -0.8 -0.6 -0.4 -0.2 0 0.2 0.4 Potential - V/SCE Curr ent demsity - A/m2 (B) (A) (C)
Fig. 2. Cyclic voltammetry performed on stainless steel electrodes (A) after 12 days’ polarisation at 100 mV vs. SCE, (B) same electrode in a fresh medium, (C) clean electrode plunged into the bioreactor at day 12; scan rate 10 mV/s.
Fig. 3. 3-D structure of anodic biofilm developed on the stainless steel electrode after 18 days’ polarisation at 100 mV vs. SCE. Biofilm thickness 80–90lm, surface area 500 500lm. (A) view in profile, (B) view from the electrode.
0 0.5 1 1.5 2 2.5 0 2 4 6 8 10 Time - Days Curr ent density - A/m 2 (A) (B) (C)
Fig. 4. Current density recorded with a microbial stainless steel electrode polarised at 100 mV vs. SCE. Biofilm (A) formed anaerobically (N2/CO2), (B) aerated, (C)
under continuous bubbling of air (aerobic conditions) for the first and continuous bubbling of N2/CO2(80/20) (anaerobic conditions) for the second. Control experiments were carried out in the same conditions but without any microbial inoculation. These control experiments did not give any current.
In both inoculated reactors under aerobic or anaerobic condi-tions, current increase was observed against time but the current recorded in anaerobic conditions was 3-times higher. After 10 days of polarisation, the current produced by the anaerobic biofilm was about 2.2 A/m2while that in the presence of air was only 0.7 A/m2. The biofilm was perfectly able to form in aerated conditions and provided significant current density (Fig. 4). At this potential value (0.1 V/SCE) on stainless steel, the direct electrochemical reduc-tion of oxygen can be neglected. The strong effect of oxygen on the current cannot be attributed to a mixed reaction on the anode, e.g. bacterial oxidation of acetate coupled to direct oxygen reduc-tion on the same electrode. The presence of oxygen consequently acted on the microbial metabolisms and on biofilm formation in an irreversible way, as no current increase was detected when the air feed was stopped. The analysis of the biofilm structure ob-tained in the presence of oxygen showed a larger amount of bio-mass (thickness >200
lm) but no other particular difference in
the structure. The capacity to implement the oxidation reaction in an aerated environment is a major advantage for the design of membrane-less MFCs or MECs. Up to now, single chamber MFCs, which have been called membrane-less, have been designed using air-breathing cathodes. Nevertheless, the anodic compartment must be in anaerobic conditions, and the air-breathing cathodes must integrate a polymeric coating (membrane, PTFE, etc.) that prevents air from penetrating into the single anodic compartment (Pham et al., 2004; Ghangrekar and Shinde, 2007; Biffinger et al., 2008; Jadhav and Ghangrekar, 2008). This coating hinders the mass transfer of protons to the cathode, and may contribute to the low performance of such cathodes by limiting proton availability. In contrast, using an anode that can work in fully aerated conditions, as was the case here, holds promise for the design of MFCs without any membrane or coating.A reactor was implemented for 10 days following the same pro-cedure with two stainless steel electrodes inside, one polarised at 100 mV/SCE and the second left on open circuit. The open circuit potential of this electrode was stable at around 250 mV/SCE. After 10 days, cyclic voltammetry was performed on each electrode at a scan rate of 10 mV/s. CV showed that only the polarised elec-trode was able to oxidise acetate, while the elecelec-trode left on open circuit generated no current in the whole range of potentials scanned (Fig. 5). The polarisation of the anode was thus absolutely
necessary to the development of an electro-active biofilm capable of catalysing the oxidation of acetate. However, biofilms with the same thickness of around 60
lm were observed on both electrodes
by microscopy at the end of the experiment (data not shown).Following the same procedure, an electro-active biofilm was formed which generated a current density exceeding 1.0 A/m2after 6 days of polarisation (Fig. 6A). The biofilm was then scraped from the anode and used as the inoculum in 500 ml of fresh seawater (10 mM acetate) to construct a new electro-active biofilm. The maximum current density was again obtained after 6 days, with a relative increase of 20% with regard to the previous biofilm (Fig. 6B). Further successive scraping and inoculation did not lead to significant improvement in the electrochemical efficiency of the biofilm. In contrast, it has been reported in the literature that successive scraping/inoculation steps can lead to large successive improvements in the current supplied at each step when inocula from bulk environments are used (Liu et al., in press). It can be con-cluded that the procedure described here, i.e. using natural biofilm as inoculum rather than samples collected from bulk sediments, al-lowed the formation of efficient biofilms with stable electrocata-lytic properties from the first step. Our previous work describing the biofilm-inoculum procedure on graphite anodes for the first time analysed the microbial population of the biofilms formed. It showed that the efficiency of the reconstructed biofilms was due to the presence of a few bacterial strains that were absent from the biofilm formed with the inoculum coming from bulk sediments (Erableet al., in press). This procedure ensured the presence of the efficient strains in the biofilm from the first construction step, in contrast to the common procedure that uses samples from bulk environments as inoculum and requires further enrichment of the efficient strains by successive scraping/inoculation steps.
Finally, the same procedure was performed with 3 electrodes in the same reactor: plain stainless steel, plain graphite and a stain-less steel grid, each of 25 cm2projected area. The maximal current densities reached under constant polarisation at 100 mV vs. SCE were 3.1, 5.9 and 8.2 A/m2, respectively (Fig. 7). Logically, using a grid multiplied the current density by a factor of around 2.5, reach-ing a current density among the highest reported at such a nega-tive potential value. The most effecnega-tive acetate-fed bioanodes reported in the literature have been obtained with air-cathode MFC systems and have reached maximal values around 8.0 A/m2 (Cheng and Logan, 2007; Fan et al., 2007with smaller systems). These works were performed using large-surface-area graphite an-odes but only the surface area of the cathode, which was smaller, was taken into account for the calculation of the current densities. This procedure is perfectly correct for comparing the efficiency of MFC systems but it fails when comparing anode performance levels, as the current density is multiplied by a factor equal to
0 0.2 0.4 0.6 0.8 1 1.2 1.4 0 2 4 6 8 10 12
Time - Days
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Fig. 6. Reconstruction of an electrochemically active marine biofilm. Current density production by initial (A) or reconstructed (B) marine biofilm on a stainless steel electrode polarised at 100 mV vs. SCE.
-3 -2 -1 0 1 2 3 4 5 6 7 -0.8 -0.6 -0.4 -0.2 0 0.2 Potential - V/SCE C u r re n t d e n si ty A /m 2
(A)
(B)
Fig. 5. Cyclic voltammograms of marine biofilms grown anaerobically for 10 days on a stainless steel electrode polarised at 100 mV vs. SCE (A) or not polarised (B); scan rate 10 mV/s.
the anode area divided by the cathode area. So, the present results cannot really be compared with the results already published. Nev-ertheless, by controlling the potential of the graphite rod anode,
Liu et al. (in press)improved the bioelectrocatalytic activity of a domestic wastewater mixed-cultures biofilm to reach 5.0 A/m2.
Stainless steel can now be considered as a promising material for building microbial anodes from natural consortia, as has previ-ously been observed with pure culture (Dumas et al., 2008b). The less obvious successes obtained previously with stainless steel an-odes in benthic fuel cells (Dumas et al., 2007, 2008c) were certainly linked to the procedure of biofilm formation, directly in MFC de-vices, which did not allow the potential value to be controlled. In consequence, the free evolution of the passive layer may have been a cause of the low current densities obtained previously. The experiments performed here with and without polarisation during biofilm formation brought out the crucial role of the potential in optimising the performance of the final anode.
4. Conclusion
Reconstructing a biofilm on a polarised stainless steel electrode from a natural biofilm used as inoculum led to remarkably efficient microbial anodes. Following this procedure, stainless steel proved to be an excellent material for designing microbial anodes that could be used in MFCs, microbial electrolysis cells, or any other biotechnological applications. Thanks to the mechanical properties of stainless steel, it should be possible to increase current density still further by using electrodes with higher specific areas, super-imposed grids, brushes or any other open structure. The capacity of the microbial anodes described here to form and to provide cur-rent in aerated environments is another major advantage for the design of membrane-less MFCs. The initial biofilm in its natural environment is exposed to air for several hours daily, which may partly explain the resistance to oxygen exhibited by the recon-structed biofilm. The description of the microbial populations gi-ven in a previous work indicated the presence of four specific strains in such reconstructed biofilms. The biofilm reconstructed in aerated conditions can be thought to contain aerobic anodophil-ic strains; we will now direct our efforts towards the identifanodophil-ication and isolation of such strains.
Acknowledgements
This research was financially supported by the European Com-munity as part of the EA-Biofilms Project (FP6, NEST508866). The authors are most grateful for the technical contributions of Luc
Etcheverry (CNRS engineer, Laboratoire de Génie Chimique, Tou-louse, France).
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