Controlled Growth of Nanostructured Biotemplates with Cobalt and

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Controlled Growth of Nanostructured Biotemplates with Cobalt and Nitrogen Co-Doping as a Binderless Lithium-Ion Battery Anode Tyler M. Huggins, Justin Michael Whiteley, Corey T. Love, Kwangwon Lee, Se-Hee Lee, Zhiyong Jason Ren, and Justin Conan Biffinger ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.6b09300 • Publication Date (Web): 16 Sep 2016 Downloaded from http://pubs.acs.org on September 19, 2016

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ACS Applied Materials & Interfaces

Controlled Growth of Nanostructured Biotemplates with Cobalt and Nitrogen Co-Doping as a Binderless Lithium-Ion Battery Anode

Tyler M. Huggins†, Justin M. Whiteley‡, Corey T. LoveΩ, Kwangwon Lee∆, Se-Hee Lee‡, Zhiyong Jason Ren*†, and Justin C. Biffinger*Ω

†

Department of Civil, Environmental, and Architectural Engineering, University of Colorado Boulder, Boulder, CO, 80309, USA ‡

Department of Mechanical Engineering, University of Colorado Boulder, Boulder, CO, 80309, USA

Ω

Chemistry Department, US Naval Research Laboratory, Washington DC., 20375, USA

∆

Department of Biology, Rutgers University, Camden, NJ 08102, USA.

Keywords: filamentous fungi, biotemplate, cobalt, nitrate, lithium

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Abstract: Biomass can serve as a sustainable template for the synthesis of carbon materials, but is limited by the intrinsic properties of the precursor organism. In this study we demonstrate that the properties of a fungal biotemplate can be tuned during cultivation, establishing a new electrode manufacturing process and ultimately improving the electrochemical performance of the biomass derived electrode. More specifically, the carbon to nitrogen ratio of Neurospora crassa mycelia mats were shifted by 5-fold while generating cobalt nanoparticles into the hyphal structure originating from macroconidia spores. This shift was achieved through nitrate limitation and equal molar concentrations of Mg2+ and Co2+ in the growth media. The resulting mycelia mat was converted via a high temperature pyrolysis process (800°C) to produce a free-standing cobalt and nitrogen co-doped electrode material with no post-modification. Ultimately nitrogen doping resulted in one of the highest recoded specific reversible capacity for a freestanding biomass derived lithium-ion anode (400 mAh g-1 at C/10). We observed an additional improvement in capacity to 425 mAh g-1 with the incorporation of 3 wt% Co. Our results show how shaping the chemical characteristics of an electrode during the growth of the biotemplate allows for sustainable carbon-based material manufacturing from a living (self-assembled) material.


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1. Introduction Energy storage is a trillion-dollar industry (in both production and hazardous waste disposal) servicing every facet of modern society.1 The rapid adoption of consumer electronics, electric vehicles, and the need for “green” energy storage, has led to a demand for renewable materials.2, 3 The use of sophisticated carbon architectures for battery electrodes, such as carbon nanotubes (CNT), doping of carbons with various heteroatoms (i.e. N, P, B,) and incorporation of transition metal nanoparticles (Co, Fe, Mn in particular), is an actively studied area in energy storage research.4-7 Advancements in material processing have been paramount in improving power densities, but often come with increased cost, energy, and resource disadvantages. In fact, it has been shown that for every kWh produced by a modern lithium-ion battery, there are more than 400 kWh in energy input required.1 In order to reduce the impact associated with advanced battery material manufacturing, many researchers have looked to nature for solutions.8, 9 Nature has provided the blueprint for many novel physical and chemical architectures that are efficiently self-assembled at the nanoscale without sophisticated nanotechniques.10 This has resulted in carbonaceous electrode materials generated from organisms ranging from viruses to crab shells.9, 11, 12 However, one of the major limitation to using native biomass as a practical electrode template are the intrinsic properties of the biological system itself.13 A majority of biomass electrode materials are created after the organism is fully formed which limits the base properties of the material. This concept has been demonstrated recently with Aspergillus aculeatus in the formation of carbon separators for Li-S batteries14 and supercapacitors.15 However, no data was presented for the modification of A. aculeatus to improve performance. Nitrogen doping4 and the encapsulation of metal oxides particles16 have been commonly used to increase the capacity and cycling stability of carbon-based lithium-ion anode materials (graphite, activated carbons, and hard carbons) in post-treatment steps. However, if an organism is manipulated at an even earlier stage of development then the final properties of the biomass can be potentially shifted to suit a particular application like nitrogen doping. Typically, archetypal fungal derived carbon materials 3 ACS Paragon Plus Environment


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are improved using several post treatment methods, including exposure of the harvested biomass to KOH17, but no studies have focused on shifting the C/N ratio at the germination phase. In this work, rather than post-treating the biomass source, we utilized the rapid production of a three dimensional hyphal structure using Neurospora crassa to produce nitrogen and metal co-doped electrodes. We demonstrate that the final nitrogen content of the biomass can be controlled by regulating the availability of free nitrate in the growth medium. We also show that Co(NO3)2 can be used as the sole nitrogen source and that the growth with cobalt nitrate facilitates the incorporation and formation of cobalt oxide nanoparticles on the biomass after pyrolysis. These binder-less free standing electrodes showed improved lithium-ion capacity correlated with the amount of nitrogen doping accomplished during the growth phase. The electrode materials as demonstrated here provides a proof-of-concept to reduce material and processing costs, while removing inactive components in lithium-ion electrodes.

2. Experimental section 2.1 Cell maintenance and isolation of conidia N. crassa wild-type strain (FGSC #262) was a gift from C. Hong (University of Cincinnati). The cells used for inoculations were stored on minimal media slants (2% Vogel’s18 50x salts, 0.01% trace elements solution, 0.005% biotin, 1.5% sucrose, and 1.5% agar) at −20 °C. Growth experiments were started from cells removed from frozen agar slants onto new agar slants incubated at 30 °C for 2–3 days in complete darkness. Conidia were isolated from slants using standard methods19 and inoculated into 100 mL of 1X Vogel’s liquid media (2% Vogel’s salts, 0.01% trace elements solution, 0.005% biotin, and 2% glucose) for batch submerged culture experiments. Conidial suspensions (1.0 mL in 1X Vogel’s medium) of OD600nm = 0.7 were used to inoculate batch growth experiments.


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2.2 Batch growth experiments Growth experiments were conducted in 50 mL of 1X Vogel’s culture media. Batch cultures were incubated at 30°C for 3-5 days (120 rpm) under constant light. The modification to the 1X Vogel’s media included defined concentrations (10 mM, 20 mM, and 40 mM) of sodium nitrate (NaNO3) or cobalt metal salts (Co(NO3)2) in comparable concentrations of NO3- anions. N. crassa growth experiments using Co(NO3)2 were performed with a 1:1 molar ratio of Mg2+ in the form of MgSO4. Experiments to determine the adsorption capacity for cobalt ions by the heat-killed biomass used autoclaved (15 min, 121°C) hyphal mats (after 72 hrs of growth) soaked in the same molar concentration of Co(NO3)2 as growth experiments with cobalt described above. Fungal mats from all experiments were collected via vacuum filtration. Fungal biomass was washed with 20 mL 1% HCl then washed thoroughly with reverse osmosis water (18 MΩ). The harvested fungal cells from all experiments were then flash frozen with liquid N2 and lyophilized for 24 hrs at 0.003 mBar.

2.3 Thermal conversion of fungal biomass into graphitic electrode Roughly ½” discs were cut out of the lyophilized biomass sheets. The lyophilized fungal biomass discs were thermally converted in a tube furnace (Thermo Scientific Lindberg Blue M Mini-Mite Tube Furnace, SSP; 208V) at 20°C min-1 to a max temperature of 800°C under N2 atmosphere. The protective gas flow rate was 100 mL min-1 and reactive gas flow rate was 10 mL min-1. Pyrolysis kinetics were also determined using a thermogravimetric analyzer (TGA) (Mettler-Toledo (TGA-DSC1); Stare software package) using the same pyrolysis conditions. The free-standing carbonized electrode was used “as-is” with no post-treatment for electrochemical measurements.

2.4 Physical and elemental characterization The morphology and structure of the fungal cells and fungal derived electrode material were investigated using scanning electron microscopy (SEM; JEOL JSM-6480LV, 30 kV). Field emission scanning electron microscopy (FE-TEM) was performed using a JEOL JSM-6500F. Elemental analysis was



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recorded using inductively coupled plasma mass spectrometry (ICP-MS) by Robertson Microlit Laboratories, Inc (Ledgewood, NJ). Microstructure for all fungal derived electrode materials were characterized by powder X-ray diffraction spectroscopy (XRD) using a Rigaku 18-Kw X-ray generator and high resolution powder diffractometer with Cu-Ka radiation derived from a rotating anode X-ray source operated at 50 kV and 200 mA. Brunauer–Emmett–Teller (BET) method using a five-point N2 gas adsorption technique (ASAP 2020; Micromeritics, Norcross, GA) was used to measure the specific surface area and pore size distribution of the fungal derived electrode materials.20 X-ray photoelectron spectroscopy (XPS) was performed using a SPECS Phobios 150MCD with Mg K source.

2.5 High performance liquid chromatography conditions Samples were collected from each batch culture at 24 hr intervals for 72 hrs. At each time point 1.0 mL of culture medium was collected and analyzed for glucose and nitrate concentration using liquid chromatography. Glucose separations were performed using a Varian Prostar HPLC with diode array and refractive index detectors. Glucose analysis was performed with a Hi-plex H+ column (300 x 7.7 mm) held at 65°C with a 5 mM H2SO4 mobile phase at 0.6 mL min-1 flow rate. Ion chromatography was performed using a Dionex ICS-3000 using a Dionex IonPac™ AS9-HC (4x250mm). The flow rate was 1.0 mL min-1 using a 9.0 mM sodium carbonate mobile phase. The concentrations of glucose and nitrate were determined independently using calibrated external standards.

2.6 Battery test conditions The carbonized biomass cores served as an electrode without modifications. The total surface area changed slightly from sample to sample as the biomass was rigid at this point. All assembly took place in a dry argon environment. The carbonized biomass, due to its conductive nature, acted as a current collector and was placed into a 2032 coin cell with a Whatman glass microfiber separator, and lithium metal foil (Aldrich, 99.99% purity) as a counter electrode. The electrolyte was 1 M LiPF6 in 1:1 (v/v) ethylene carbonate/diethyl carbonate (Aldrich). The carbon and cobalt-containing carbon electrodes were first lithiated (discharged) to 0.005 V versus the lithium metal foil at a rate of C/20. The charge voltage 6 ACS Paragon Plus Environment

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cutoff was 2.0 V. Each electrode was cycled between 0.005 – 2.0 V for 10 cycles at a rate of C/10, then increased for subsequent cycling at C/5 (1C = 370 mAh g-1 for pristine graphite). Galvanostatic operation took place on an Arbin BT2000 Battery Test Station.

3. Results and Discussion 3.1 The growth of N. crassa to control chemical composition

Figure 1. (a) Photograph of N. crassa growth after 48 hours, (b) SEM image of hyphal mat, (c) graphical illustration of biomass thermal conversion, (d) SEM image of carbonized hyphal mat, (e) SEM image of biocarbon tube, and (f) FETEM image of cobalt nanoparticles.

We used Neurospora crassa, a biotechnologically relevant filamentous fungus, as the living template for electrode fabrication based on its robustness in minimal nutrient media, high tolerance to an assortment of toxic metals,21, 22 and its rapid linear growth rate of 3-6 mm h-1 per hyphal tip from conidial spores.23, 24 Figure 1 shows the different qualitative stages of this research starting from a filamentous fungal mats (Figure 1A) and the 3D hyphal structures observed using the dried hyphal mats (Figure 1B) to the carbon-based structures observed after pyrolysis (Figures 1C-D and Figure S1).



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Inoculation of the growth medium with macroconidia spores generates fungal mats. After inoculation, we focused on manipulating the natural response of N. crassa to nitrate limitation to tune the chemical composition of the biomass toward improved Li-cycle capacity. This included control over the final C/N ratio (Table 1) calculated from elemental analysis of the mycelia biomass pre- and postpyrolysis. Glucose was used as the sole carbon source for submerged cultures and mycelia mats were formed in constant light at 25°C. These growth conditions resulted in reproducible fungal mat formation with the rapid propagation of conidial spores for all experiments over 72 hrs. The typical composition of the medium was based Vogel’s formulation containing 20mM NH4NO3. Since both ammonium25 and nitrate26 are viable nitrogen sources for N. crassa, we used the 20 mM NH4NO3 growth results using to compare how the formation of the mycelia mat changed by imposing a nitrate limitation. The final C/N ratio for the fungal mat generated from 20 mM NH4NO3 was 9.1 ± 0.3. Nitrate was also consumed approximately 2x faster than ammonium using ammonium nitrate and both ions were not completely consumed when the mycelia mats were harvested (raw ion chromatography data not shown). The form of the nitrogen source is important since the presence of ammonium can repress nitrate assimilation pathways transcriptionally in N. crassa26, 27 however these potential mechanistic changes28 were not evident in the form of the final graphitic material. Since one of the goals was to limit nitrogen availability while incorporating cobalt at the growth phase, only sodium nitrate salts were chosen for shifting the C/N ratio during germination. These data confirm that using nitrate salts alone does not limit the amount of biomass generated nor effect the C/N ratio when in excess. In addition, excess sodium nitrate (40 mM) did not result in a material with a higher C/N ratio compared to 20 mM NH4NO3 confirming that both ammonium and nitrate are being used to create the same structural material. However, the use of ammonium could potentially influence the amount of cobalt uptake and thus it was removed from the media formulation. The mass of overall bulk dried biomass when replacing the typical 20mM NH4NO3 with 40 mM NaNO3 was 100 ± 2 mg and 92 ±


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2 mg, respectively. The C/N ratio resulting from growth with 40mM NaNO3 was slight higher than growth using 20 mM NH4NO3 (Figure 2 and Table 1). Based on these growth results, the concentration of nitrate was reduced to 20 mM (NO-20) and ultimately 10 mM (NO-10), in the culture medium. The rate of nitrate consumption using our experimental conditions was 0.8 ± 0.1 mM nitrate/h. Our results showed that these subsequent nitrate limitations imposed on N. crassa decreased the level of nitrogen doping by 26% using 20mM NaNO3 (Figure 2A) because the rate of biomass formation was unaffected by the nitrate limitation at that concentration. This result makes it possible to tune the C/N ratio of the final biomass material. This was not true for growth using 10 mM nitrate since the rate of macroconidia propagation decreased by approx. 50% and only a slightly higher C/N ratio was observed. Controlling the amount of heteroatom doping in this way will affect the structural and electrochemical environment of coordinated metals of the final electrode material. The biomass formed with excess nitrate in this work (regardless of the nitrogen source) resulted consistently in a C/N ratio of approx. 9-10 regardless of the nitrogen source. Our results indicate that the ability of N. crassa to continue to grow (without significantly affecting the growth rate) after the complete consumption of sodium nitrate was the key to shifting the C/N ratio of the final material. Using this method, the C/N ratio of the raw material was shifted from 9 using 40 mM sodium nitrate to as great as 15 using 10 mM sodium nitrate in the growth medium (Table 1). Typically, with carbonaceous materials the introduction of a heteroatom like nitrogen can be accomplished with post-processing using ammonia.29 Even the pyrolysis of sucrose and ammonium nitrate alone can generate capacitors consisting of a 3% nitrogen-doped material.30 In Agaricus sp., control over the nitrogen to carbon ratio in a fungal-derived capacitor was accomplished using a caustic KOH post-processing step.17

Their processed biochar had a C/N ratio of as

high as 41 and could be as low as 13 but required a defined balance between KOH/biomass weight percentages.



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Not only could limiting nitrate during growth effect the properties of the final material but also provides a method to incorporate metal ions into the final biomass. N. crassa has been shown to remain viable when exposed to 0.4 to 6.0 mM concentrations of toxic metals such as Zn(II), Ni(II), and Co(II).3133

Transition metal oxides are currently being investigated in rechargeable battery technologies34 but

many of these same metals (Co, Mn, Ni) are toxic to a majority of microorganisms. In order to incorporate Co(II) into the biomass directly during the growth of N. crassa and ultimately into the carbon matrix of the electrode, we cultured the fungus in the presence of 10 mM Co(NO3)2 without any additional nitrogen source. The toxicity of cobalt was mitigated by using equal molar concentrations of Mg2+ which also did not affect the growth rate (Figure S2). A C/N ratio of 10 ± 1 was observed from growth experiments that used Co(NO3)2. This C/N ratio was comparable to results from growth experiments with excess nitrate (Figure 2A). Ion chromatography confirmed that the fungal mats formed with Co(NO3)2 were not nitrate limited because the formation of the fungal mat in the presence of cobalt was 40% slower and thus there was less mass formed when the mat was collected. There was no significant accumulation of magnesium in the material even though Mg2+ was required to mitigate the toxicity of cobalt based on our growth experiments (Figure S2). Magnesium has been shown to decrease the effects of cellular toxins on Cercospora beticola35 or Fusarium graminearum36 by increasing cell wall conductance which might play a role in the tolerance of conidial spores to such a high concentration of cobalt. Magnesium can also reverse cobalt transport in wild type N. crassa through inhibiting surface binding31, 33 but our results indicate that cobalt binding was not inhibited by the the equal molar concentration of magnesium required for growth. Whether N. crassa is using an avoidance or tolerance mechanisms for survival in excess metals,37 magnesium can be used to balance maximizing the rate of the fungal mat formation to the concentration of cobalt taken up by the mat during growth. The weight percentage of cobalt in the graphitic material generated when N. crassa was cultured with 10 mM Co(NO3)2 was 2.3% (FCCE) which was significantly higher than the amount of cobalt 10 ACS Paragon Plus Environment

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absorbed when autoclaved mycelia were used as a general cobalt biosorbent (FCCE-S) (0.84%; Table 1). These data indicate that even though the total mass formed was less using cobalt nitrate during germination (and could be potentially overcome with slight longer growth periods or higher temperatures), the concentration of cobalt in FCCE was increased by 3-fold compared to the same fungal mat being used as a general metal sorbent (FCCE-S). Even though the C/N ratio remained the same between FCCE and FCCE-S carbonized electrodes (Table 1), the Co/N ratio was four times greater for FCCE (0.42 ±0.05) compared to FCCE-S (0.11± 0.01). This difference can be attributed to exposing the actively growing fungal hyphae to Co(NO3)2 and potentially different Co-N binding modes present in FCCE compared to FCCE-S. Table 1. Elemental composition (w/w) of biomass and anode material generated from N. crassa fungal mats cultured with 10mM Co(NO3)2 (FCCE), autoclaved fungal mats soaked with 10mM Co(NO3)2 (FCCE-S), 40mM NaNO3 (NO-40), 20mM NaNO3 (NO-20), and 10mM NaNO3 (NO-10). Dried Biomass

After Pyrolysis BET

C%

H%

N%

Co %

C/N

C%

H%

N%

Co %

FCCE

43 ± 2

6.3 ± 0.3

6.4 ± 0.3

0.38 ± 0.02

10 ± 1

55 ± 2

0.83 ± 0.04

5.5 ± 0.3

2.3 ± 0.1

5.9 ± 0.3

FCCE-S

40 ± 2

5.9 ± 0.3

6.2 ± 0.3

0.13 ± 0.01

11 ± 1

76 ± 4

0.76 ± 0.04

6.9 ± 0.3

0.80 ± 0.04

3.9 ± 0.2

NO-40

39 ± 2

6.1 ± 0.3

6.4 ± 0.3

-

9.7 ± 1

63 ± 3

1.9 ± 0.1

6.5 ± 0.3

-

4.3 ± 0.2

NO-20

46 ± 2

7.1 ± 0.4

4.9 ± 0.2

-

13 ± 2

67 ± 3

1.4 ± 0.7

5.1 ± 0.3

-

1.4 ± 0.1

NO-10

45 ± 2

5.4 ± 0.3

3.3 ± 0.2

-

15 ± 1

67 ± 3

2.1 ± 0.1

4.5 ± 0.2

-

1.7 ± 0.1

Sample

2 -1

(m g )



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Figure 2. (a) Nitrate consumption (grid pattern) by N. crassa after 48 hour mycelial growth using 40 mM NaNO3 (NO-40; purple), 20 mM (NO-20; blue), and 20 mM NH4NO3 (NH-20; orange) and subsequent C/N ratio (horizontal line pattern). (b) Comparison of the C/N horizontal line pattern). (b) Comparison of the C/N (horizontal line pattern) and biomass production (solid) using 10 mM Co(NO3)2 (FCCE) (green) and N0-40 soaked in 10 mM Co(NO3)2 (FCCE-S).

3.2 Pyrolysis of N. crassa and the formation of binder-free electrodes Pyrolysis can transform disordered chemical micro-structure into a more ordered turbostratic material.38 The thermal conversion of fungal mats into graphitic materials was accomplished under a nitrogen atmosphere. Identical heating cycles were used to convert the dried biomass generated from growing N. crassa in 10 mM (NO-10), 20 mM (NO-20), and 40 mM (NO-40) sodium nitrate, 10 mM cobalt nitrate (FCCE), or the absorption of cobalt by pre-grown and autoclaved mycelia soaked in cobalt nitrate (FCCES) into free-standing electrodes. Pyrolysis of each material was performed using 80-100 mg of vacuum-


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dried (lyophilized) biomass. The typical thermogravimetric result from the pyrolysis of all materials from room temperature to 800°C at a rate of 20°/min is shown in Figure S3. Based on thermogravimetric data (and differential data) a major weight loss event occurred around 300°C with a total weight loss of 80% once 800°C was reached. Neither the presence of cobalt in the material nor large shifts in the C/N ratio resulted in a significant change in the thermal conversion events. The temperature range (180-450°C) where this weight loss event occurred is consistent with the decomposition of proteins and of raw materials with high cellulosic content contained in other biomass sources.39 The graphitic material after pyrolysis was a free-standing structure and maintained the 3D pore integrity of the parent material determined by SEM (Figure 1D and Figure S1). The average pore volume for each electrode was around 1100 Å (Figure S4) and resulted in a low (1-5 m2 g-1) Brunauer-EmmettTeller (BET) surface area (Table 1). The materials that were limited in nitrate during growth (NO-10 and NO-20) showed significantly lower surface area than all other materials but this difference was not due to changes in the 3D pore structure observed using SEM. Higher surface area materials could be produced if the lyophilisation step was removed but this comes at the cost of losing the advantage of the natural 3D structure of the material.

Figure 3. XRD spectra of FCCE (green), FCCE-S (gray) and NO-40 (purple) illustrating the dominant carbonate peaks. 13 ACS Paragon Plus Environment


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The XRD spectra shown in Figure 3 confirms the graphitic nature of cobalt cultured biochar (FCCE), cobalt soaked biochar (FCCE-S), or with excess nitrate (NO-40) from the broad reflections between 15-35° indicative of small domains of coherent stacking.40 The presence of MgCO3 (at 34°) was observed with only the NO-40 material and was absent in the materials exposed to cobalt which is interesting considering excess magnesium was used only in FCCE and FCCE-S experiments. The form of cobalt in both the FCCE and FCCE-S materials was tentatively confirmed to be Co2O3 by XRD and high resolution transmission electron microscopy (TEM). It was difficult to acquire enough signal from the cobalt nanoparticles to generate elemental maps of the hyphal surface because of the average 2-5 nm size of the Co2O3 nanoparticles (Figure 1F). Interestingly, these cobalt nanoparticles were only observed in the carbonized hyphal structures grown with cobalt nitrate (FCCE) but not soaked with cobalt nitrate after growth (FCCE-S). Plants, bacteria, and fungal biomass have been used extensively for the removal of heavy metals from the environment.41 The mechanisms of biosorption are primarily based on chemical interactions of metal ions and the functional groups present on the cell surface, such as electrostatic interactions, ion exchange, and metal ion chelation or complexation.42 Biosorption capacity is greatly affected by the chemical makeup of the cell wall and surface area. In addition to cell wall interactions, living cells can also actively take up metal ions from the environment, but often only to a maximum threshold before it becomes toxic.43 X-Ray photoelectron spectroscopy (XPS) was performed on all of the graphitic materials used for Li-cycle experiments to determine how the surface characteristics of the materials exposed to cobalt were effected after growth. The bioaccumulation of cobalt during growth (FCCE) was compared to soaking the fungal mat (FCCE-S) and our results indicate that different binding modes were established. Fungal biomass generated without cobalt, for example the 40-NO (Figure 4; bottom row) and FCCE-S materials (Figure S6), showed spectral C1s features dominated by aromatic carbons in both sp2 (49%; 283.8 eV) and sp3 14 ACS Paragon Plus Environment

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(32%; 284.8 eV) with smaller concentrations of C-N/C-O (12%; 286.2 eV) and C=O (4%; 288.8 eV). High aromatic carbon abundances are traits indicative of condensation in the carbon structure and the development of a graphitic-like patterns.44 The material that was grown with cobalt (FCCE) had the majority of aliphatic C binding but a much less intense sp2 peak (19%), and higher C-N/C-O concentration (21%). The NO-40 and FCCE-S materials also shared similar peak intensities for the O1s spectrum with 43% O-C (533.2 eV), 37% O-NC (532.0 eV), and 20% O=C (531.1 eV) oxygen binding modes, while FCCE was primarily dominated by O-C (52%). The contribution to increased sp3 (50%) and C-N/C-O can be attributed to the higher Co and lower C concentrations for FCCE materials compared to both NO-40 and FCCE-S materials. For the N 1s spectrum, all three materials were primarily composed of pyridinic (N1: 398.7 eV) and pyrrolic (N3:401.1 eV) aromatic N bonding which ultimately creates a more conductive carbon material (Figure 4). The major difference between FCCE electrodes was the average 10% increase in pyridinic N bonding compared to NO-40 and FCCE-S electrodes and indicates that cobalt exposure resulted in this shift. The spectra for the cobalt oxygen binding are shown in the supporting information were not significantly different between FCCE and FCCE-S (Figure S5). However, there was an increase in Co/N ratio that resulted from the germination of the macroconidia with Co(NO3)2. The combination of XRD, XPS, and elemental data confirm that even though this shift in Co/N ratio was not observed with data focused directly on cobalt binding (Figure 3 and Figure S5) there was a significant difference in Co binding to the hyphae that was evident in the electrochemical performance of the FCCE electrodes in lithium cycling experiments.



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Figure 4. X-ray photoelectron spectroscopy of FCCE (green) and NO-40 (purple) graphitic electrodes. N 1S labels are N1: pyridinic; N2: amine or imine; N3: pyrrolic; N4: quaternary; N5: pyridinic-N-oxide.

3.3 Electrochemical performance of fungal electrodes as Li-ion battery anode The free-standing binder-less electrodes that resulted from pyrolysis were evaluated as an anode material without any further post-processing. The carbonized biomass was free-standing which allowed for the graphitic disc to be used as an electrode without the addition of conductive chemical binders (Figure 1C) or use of any extra current collector. The ability of the carbonized material to be used as a stand-alone electrode provides numerous advantages such as cutting out expensive electrode processing steps, and increasing overall electrode based capacity. Most lithium-ion graphite electrodes use approx. 10% extra materials (binder + conductive additive)45, therefore the fungal-derived electrodes already maintain a distinct advantage in electrode based capacity. The XPS spectra in Figure 4 showed that pyridinic and pyrrole nitrogen functionality is fully incorporated into the graphitic structure and tuned with the amount of NaNO3 in the growth media. The cycling behavior of the biomass generated from nitrate limitation (NO-10, NO-20, NO-40) is shown in Figure 5. The first cycle voltage profile and associated dQ/dV are displayed in Figure 5B and 5C. All


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three samples achieve greater capacity than theoretical for graphite (372 mAh g-1); therefore, the samples are more analogous to nitrogen-doped carbons – a class of well-documented potential battery materials.4648

An irreversible peak is present in all samples around 0.8 - 0.9 V that disappears with subsequent cycles. This is attributed to the formation of a solid electrolyte interphase (SEI) layer and consistent with other hard carbon materials in organic lithium electrolytes.49 An effective way to mitigate this lithium loss at the carbon anode is through the incorporation of film-forming electrolyte additives such as vinylene carbonate but is outside the focus of this work.50 With increasing nitrogen content, the first cycle coulombic efficiency decreases (NO-10: 72%, NO-20: 59%, NO-40: 50%), matching the trend in the literature for other nitrogen-doped soft carbons.45-48 After several cycles, the samples stabilize near 400 mAh g-1 at a rate of C/10. The voltage profile and dQ/dV for cycle 10 is displayed in Figure 5D and 5E. The charge characteristics show similarities between NO-10 and NO-20 and change quite differently for NO-40. Once the cycling rate was increased to C/5, only a small dip in capacity was observed yet stabilization occurs almost immediately with all samples generating an average coulombic efficiency close to 100%. The low initial Coulombic efficiency observed with NO-10, NO-20, and NO-40 electrodes is due to the high surface area and porosity of the as-synthesized materials that is commensurate with other bioderived carbons (49 and 57%).51 By the 5th cycle, the efficiency is near 100% which is consistent with the findings of Abraham where impedance spectroscopy was used to identify a robust SEI on graphite after 5 cycles.52 The best performing nitrogen-doped material, NO-40 achieves a stable capacity of near 350 mAh g-1 for 100 cycles. When compared to commercial graphite, this is higher on an electrode-based capacity (372 mAh g-1) minus 10% for all other components and does not include current collector.



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Figure 5. (a) Galvanostatic discharge/charge characteristics of nitrogen-doped, free-standing, fungal mats carbonized at 800°C. All three samples underwent lyophilization before pyrolysis. 0.005 - 2 V voltage range. (b) 1st cycle voltage profiles for three three samples at a rate of C/20. (c) Differential capacity plot of 1st cycle. (d) 10th cycle voltage profiles for three samples at a rate of C/10. (e) Differential capacity plot of 10th cycle.

In comparison to other fungal-derived electrodes, this charge/discharge behavior compares very well and actually appears more notable once the voltage window is taken into consideration. Most hard carbons in the literature are cycled up to 3 V in a half-cell.11, 53 While generating large capacities, this is 18 ACS Paragon Plus Environment

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an unusable threshold as it would generate an extremely low voltage in a full-cell and render the inherent capabilities of lithium-ion useless. For the three cobalt-free samples, in particular NO-10 and NO-20, the majority of capacity is derived at less than 1 V, far exceeding other soft carbons and nitrogen-doped carbons. In order to demonstrate stability in the low voltage region for the Cobalt-free electrodes, the same cycling test was performed between 0 and 1 V (Figure S7). In this test, lyophilization was not used to dry the material prior to pyrolysis to compare the effect on the material. Stability was achieved at C/5 with NO-40 having the highest capacity of 200 mAh g-1. It is clear, however, the improvement lyophilization has upon the cycling behavior of the final electrode. Specifically, the improvement of the first cycle efficiency and greater capacity retention at higher rates. This is in accordance with other nano-structured electrodes providing greater capacities at higher rates through larger surface areas.11 The lyophilized versions of the electrode exhibit faster stabilization within the first few cycle compared to unlyophilized counterparts. This could indicate that the more open framework plays a key role in assisting wetting of the electrolyte and transport of lithium to surfaces easier. We anticipate the ability to improve upon this stabilization region (cycles 1 to 10) even further by optimizing the electrode processing by rolling the fungal mats to a consistent size or growing the fungus into a more reproducible geometry. These possibilities will the subject of a future study. The Co(NO3)2 grown fungal mats (FCCE) provide an opportunity to impregnate the carbon structure with a high capacity conversion material. Transition metal oxides have been investigated recently as potential anode candidates due to lower voltages and high theoretical capacities.54 It was demonstrated that in order to achieve successive reversibility, the metal oxide should have a sufficiently nano domain size to allow for the reformation upon delithation.55 Materials such as CoO and Co3O4, with and without anchoring to graphite, have been extensively studied.55 Figure 6 shows the cycling behavior of the fungal-derived materials grown in Co(NO3)2 (FCCE) or soaked in Co(NO3)2 (FCCE-S), respectively. FCCE electrodes demonstrates stable capacity at C/10 of 425 mAh g-1, an increase over the 19 ACS Paragon Plus Environment


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nitrogen doped samples. As only a small percentage of Co is detected by elemental analysis but the highest Co/N ratio was observed, this improvement is theoretically feasible.

Figure 6. (a) Galvanostatic discharge/charge characteristics of cobalt infused fungal mats and cobalt soaked fungal mats, FCCE and FCCE-S, respectively. (b) 1st through 10th cycle voltage profiles of the FCCE material. In contrast, the FCCE-S (soaked) electrodes do not demonstrate an increase in capacity and have a lower first cycle CE (43%) than the cobalt-free nitrogen doped electrodes (Figure 5). Since, cobalt is detected by elemental analysis in the soaked materials but the Co/N ratio was significantly less than FCCE, a possible justification is that any remaining cobalt oxide is contained on the surface of the biomass, which would not allow the oxide to reform on charging. Whereas, small domains of cobalt oxide are detected in FCCE and thus are fully encapsulated. The stable capacity of FCCE is then able to remain at a high value compared to the soaked biomass (Figure 6B). Unfortunately, the cobalt oxide conversion reaction voltage overlaps with the nitrogen-doped carbon voltage profile and cannot be precisely placed on the voltage profile.55 However, the higher capacity is retained throughout long-term cycling at C/5. This indicates that the Co2O3 is likely fully encapsulated in the carbon material as it can continually reform and cell resistance does not increase due to side reactions (Figure 6B). We anticipate that growth of a filamentous fungi in toxic metals is well suited to tackle some of the underlying issues with hard carbons as lithium-ion anode materials: low first cycle CE, few cycle stabilization on onset. As we have the ability to adjust material properties from growth, we anticipate an


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improvement to first cycle CE by incorporating lithium either through growth in a lithium containing solution or performing a wash with lithium species after growth.

4. Conclusions A free-standing binder-free electrode was created from Neurospora crassa fungal mycelia after pyrolysis. The C/N ratios of the fungal materials were controlled at the growth phase starting with macroconidia spores under nitrate limitation which imparted significant changes in the Li-cycling behaviour of the electrodes. Ultimately, N. crassa cultured with Co(NO3)2 generated well dispersed 2-5 nm cobalt oxide nanoparticles while fungal mats soaked in Co(NO3)2 did not results in nanoparticles after pyrolysis. These results conclude that alterations during the growth phase of fungal biomass can result in improved electrode material properties compared to electrodes created from fungal mats treated as general biosorbents. The battery performance measurements from this study are among the highest recorded for a freestanding biomass derived lithium ion anode material and the first for N. crassa.

Associated Content Supporting information contains growth, thermogravimetric data, SEM images, XPS of FCCE and FCCES, pore volume data for FCEE and NO-40 materials, and Li-cycling behavior without lyophilization.

Author Information Corresponding Authors *E-mail: [email protected] *Email: [email protected]



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Acknowledgements This work was supported by the ONR NURP program led by Maria Medeiros. We thank Chris Hong from the University of Cincinnati for providing the wild type strain and helping establish the initial protocols for culturing and manipulating Neurospora crassa. We also thank B.J. Ward for the BET analysis and the CSU Central Instrument Facility for aiding in material surface analysis and Thomas Boyd (NRL) for his help with ion chromatography.

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TOC figure:


Controlled Growth of Nanostructured Biotemplates with Cobalt and

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