Simultaneous recovery and separation of rare earth elements in ferromanganese nodules by using Shewanella putrefaciens

    Simultaneous recovery and separation of rare earth elements in ferromanganese nodules by using Shewanella putrefaciens Jun Fujimoto, Kazuya Tanaka, Naoko Watanabe, Yoshio Takahashi PII: DOI: Reference:

S0304-386X(16)30200-6 doi: 10.1016/j.hydromet.2016.09.005 HYDROM 4434

To appear in:

Hydrometallurgy

Received date: Revised date: Accepted date:

26 April 2016 17 August 2016 24 September 2016

Please cite this article as: Fujimoto, Jun, Tanaka, Kazuya, Watanabe, Naoko, Takahashi, Yoshio, Simultaneous recovery and separation of rare earth elements in ferromanganese nodules by using Shewanella putrefaciens, Hydrometallurgy (2016), doi: 10.1016/j.hydromet.2016.09.005

This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

ACCEPTED MANUSCRIPT

Simultaneous recovery and separation of rare earth elements in ferromanganese nodules

IP

T

by using Shewanella putrefaciens

1

SC R

Jun Fujimoto1, Kazuya Tanaka2,3*, Naoko Watanabe2 and Yoshio Takahashi1,4

Department of Earth and Planetary Systems Sciences, Graduate School of Science,

Institute for Sustainable Sciences and Development, Hiroshima University, 1-3-1

MA

2

NU

Hiroshima University, 1-3-1 Kagamiyama, Higashi-Hiroshima, 739-8530, Japan

Kagamiyama, Higashi-Hiroshima, 739-8530, Japan Advanced Science Research Center, Japan Atomic Energy Agency, 2-4 Shirakata,

Department of Earth and Planetary Science, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo Bunkyo-ku Tokyo, 113-0033, Japan

CE P

4

TE

D

Tokai, Ibaraki 319-1195, Japan

AC

3

Revised version August 17, 2016

* Corresponding Author: Kazuya Tanaka E-mail address: [email protected] Phone: +81-29-284-3518 Fax: +81-29-282-5927

1

ACCEPTED MANUSCRIPT

Abstract

T

Rare earth elements (REEs) are used in various advanced materials including

IP

catalysts, alloys, magnets, optics, and lasers. REE resources are unevenly distributed

SC R

around the world, which continues to cause geopolitical concerns. Thus, securing REE resources has become an important subject for the sustainable development of industry and society. In this study, we investigated ferromanganese (Fe-Mn) nodules and crusts

NU

as a REE resource because they contain high REE concentrations and are widely

MA

distributed on the seafloor in the Pacific Ocean. We examined recovery of REEs in Fe-Mn nodules by using Shewanella putrefaciens (Fe-reducing bacterium). In this method, Fe-Mn nodule decomposition and REE recovery were achieved simultaneously

TE

D

in a single solution system. Fe-Mn nodules were reductively decomposed in NaCl solution under anaerobic conditions with daily addition of sodium lactate as an electron

CE P

donor. During the decomposition of Fe-Mn nodule, REEs released from the Fe-Mn nodule were adsorbed on bacterial cells. Light REEs had higher adsorption rates on

AC

bacterial cells than heavy REEs, which was possibly due to complexation with sodium lactate and carbonate produced by bacterial activity. Of the conditions studied here, the best REE adsorption rates were obtained with 0.5 M NaCl solution at pH 7 with daily addition of 1 mmol sodium lactate. Most of the REEs adsorbed on the bacterial cells were recovered by leaching with 0.01 M HCl. The reductive dissolution of Fe-Mn nodules using Fe-reducing bacteria is a promising environmentally friendly method for recovering REEs from Fe-Mn nodules and crusts.

Keywords: ferromanganese nodule, rare earth elements, Fe-reducing bacteria, adsorption, reductive dissolution 2

ACCEPTED MANUSCRIPT

1. Introduction

T

Rare earth elements (REEs), namely, Sc, Y, and lanthanides, have been used to

IP

produce various advanced materials and technologies such as catalysts, alloys, magnets,

SC R

optics and lasers (Eliseeva and Bünzli, 2011). Many minerals containing REEs as the main components occur in ore deposits worldwide (Kanazawa and Kamitani, 2006). There are the two largest carbonatite-hosted deposits, Bayan Obo in China and

NU

Mountain Pass in USA, characterized by light REE enrichment (Kanazawa and

MA

Kamitani, 2006; Mariano and Mariano, 2013). The ore grades of Bayan Obo and Mountain Pass were estimated to be 6 and 8wt%, respectively, as total REE oxides. In contrast, ion-adsorption REE ore deposits show heavy REE enrichment (Wu et al.,

TE

D

1990), and the deposits are mainly distributed in southern China. Ion-adsorption ores have the advantage that REEs can be readily extracted with ammonium sulfate solution.

CE P

REE phosphate minerals, monazite and xenotime, are also found in REE mineral ores (Kanazawa and Kamitani, 2006; Mariano and Mariano, 2013). These types of REE

AC

resources are unevenly distributed globally, which is a major geopolitical concern (Eliseeva and Bünzli, 2011). Therefore, to maintain a stable supply of REEs to industry, it is important to ensure there are a variety of REE resources. Here, we propose ferromanganese (Fe-Mn) nodules and crusts as a new REE resource. Fe-Mn nodules and crusts are ubiquitous in the Pacific Ocean, and nodules are widely distributed on seafloors and crusts on the slopes of seamounts (Bau et al., 1996; Hein et al., 2003; Takahashi et al., 2007). Fe-Mn nodules and crusts are mainly composed of Mn(IV) oxide and Fe(III) oxyhydroxide, to which REEs are strongly adsorbed (Ohta and Kawabe, 2000, 2001). REEs in seawater have been incorporated into Fe-Mn nodules and crusts during their growth over a geological timescale 3

ACCEPTED MANUSCRIPT

(Takahashi et al., 2007). Therefore, REEs are enriched in Fe-Mn nodules and crusts with

T

total REE concentrations of up to 1000-2000 mg/kg despite the low REE concentrations

IP

in seawater (De Carlo and McMurtry, 1992; Piepgras and Jacobsen, 1992; Bau et al.,

SC R

1996; Zhang and Nozaki, 1996; Ohta et al., 1999; Takahashi et al., 2007). The marine Fe-Mn nodules and crusts have significantly lower grades of REEs than land-based REE mines such as carbonatites. However, the total tonnage of the marine Fe-Mn

NU

deposits is much larger than land-based deposits. Therefore, Hein et al. (2013) pointed

MA

out that the tonnages of total REE metals are comparable in Fe-Mn nodules and crusts with the two largest carbonatite-hosted deposits, Bayan Obo and Mountain Pass. Furthermore, they emphasized that Fe-Mn crusts and nodules have respectively, 18%

TE

D

and 26% heavy REEs of the total REEs, whereas the large terrestrial REE deposits have <1% heavy REEs. This can be an advantage of Fe-Mn nodules and crusts because heavy

CE P

REEs have a much greater economic value. However, Fe-Mn nodules and crusts have not been exploited because of the following two problems. First is the cost-effective

AC

collection of Fe-Mn nodules and crusts from deep seafloors. Second, is the lack of effective methods for recovering REEs from Fe-Mn nodules and crusts. Here we focused on the second point, recovery of REEs from Fe-Mn nodules and crusts. The technological problems of addressing the first point are beyond the scope of this study. The recovery process is divided into two steps. First, Fe-Mn nodules are decomposed and dissolved with acids such as HCl, HF, and HNO3 (Bau et al., 1996; Ohta et al., 1999; Takahashi et al., 2007). Then, the REEs in solution are separated from the other metallic elements to be purified by ion exchange and organic solvent extraction (e.g., Gupta and Krishnamurthy, 2004). However, a large amount of acid and organic solvent would be required to deal with Fe-Mn nodules and crusts on an 4

ACCEPTED MANUSCRIPT

industrial scale. Therefore, a more environmentally friendly method is needed to use

T

Fe-Mn nodules and crusts as REE resources.

IP

Bioleaching with Fe-oxidizing bacteria has been used for oxidative dissolution of

SC R

metal sulfides in many studies (Sand et al., 2001; Tributsch, 2001; Vera et al., 2013), and the method may also be suitable for reductive dissolution of Fe and Mn oxides. Some bacterial species, called Fe-reducing bacteria, can obtain energy for growth by

NU

coupling various organic compounds as an electron donor to dissimilatory Fe(III) or

MA

Mn(IV) reduction (e.g., Lovley et al., 1989; Dollhopf et al., 2000). Lee et al. (2001) reported that Fe-Mn nodules can be decomposed by incubating with Fe-reducing bacteria under anaerobic conditions. Dissolution of Fe-Mn nodules by Fe-reducing

TE

D

bacteria is associated with the release of metallic elements, including REEs, from the nodules into solution. Takahashi et al. (2005, 2010) reported that dissolved REEs in

CE P

aqueous solution were strongly adsorbed on the surfaces of bacterial cells. Therefore, we expect that REEs released from Fe-Mn nodules would be re-adsorbed on the

AC

surfaces of bacterial cells if Fe-reducing bacteria were incubated in a medium containing Fe-Mn nodules and organic matter under anaerobic conditions. In other words, Fe-Mn oxide decomposition and REE recovery could be achieved simultaneously in a single solution system with Fe-reducing bacteria. At the same time, other metal resources such as Co, Ni, Cu, Zn, and Pb, which are enriched in Fe-Mn nodules, would also be recovered by decomposition of Fe-Mn nodule. In this work, we examine the environmentally friendly recovery of REEs, Co, Ni, Cu, Zn, and Pb from Fe-Mn nodules with Fe-reducing bacteria.

2. Materials and methods 5

ACCEPTED MANUSCRIPT

Experimental steps are shown in Fig. 1, and details in each step are described

T

below.

IP

2.1. Fe-Mn nodule

SC R

Fe-Mn nodules are classified according to their origin as hydrogenetic (HG), diagenetic (DG), or hydrothermal (HT) (Dymond et al., 1984; Takahashi et al., 2007). In general, REE concentrations are higher in HG nodules than in DG and HT nodules

NU

(Ohta et al., 1999; Takahashi et al., 2007), indicating that HG nodules are superior as a

MA

REE resource. We selected a HG sample, D535, collected during cruise GH83-3 of the Hakurei-maru (Usui et al., 1994). The chemical composition of D535 including REEs is

TE

D

shown in Table 1.

2.2. Cultivation of Fe-reducing bacterium

CE P

We used Shewanella putrefaciens, a Fe-reducing bacterium, for reductive dissolution of Fe-Mn nodules (Dollhopf et al., 2000; Suzuki et al., 2014). S. putrefaciens

AC

NBRC3908 was obtained from the National Institute of Technology and Evaluation (Tokyo, Japan). We prepared a liquid medium containing 10 g/L of polypeptone (Nihon Pharmaceutical Co., Ltd., Tokyo, Japan), 2 g/L of yeast extract (Oxoid Ltd, Basingstoke, UK), and 0.5 g/L of MgSO4·7H2O (Suzuki et al., 2014). Polypeptone, yeast extract, and MgSO4·7H2O were dissolved in artificial seawater (375 mL) diluted with ultrapure water (125 mL; total of 500 mL). The artificial seawater was prepared by dissolving Daigo’s artificial seawater SP for Marine Microalgae Medium (Wako Pure Chemical Industries, Osaka, Japan) in ultrapure water. The medium was divided into 50 mL fractions in glass flasks, and then sterilized in an autoclave at 121°C for 15 min. S. putrefaciens was precultured aerobically in the medium at 30°C on a rotary shaker at 6

ACCEPTED MANUSCRIPT

100 rpm for 24 h. Then, the liquid medium was inoculated with the precultured bacterial

T

cells and incubated at 30°C for 24 h.

IP

The bacterial cells were harvested by centrifugation, followed by washing three

SC R

times with 0.01, 0.1, or 0.5 M NaCl solution corresponding to the conditions of the subsequent bioleaching experiments. The cleaning NaCl solutions were buffered with 20 mM 2-[4-(2-Hydroxyethyl)-1-piperazinyl]ethanesulfonic acid (HEPES) at pH 7 or

NU

20 mM 2-Morpholinoethanesulfonic acid (MES) at 5.5, 6, or 6.5. The washed bacterial

MA

cells were suspended and adjusted to the desired density in the HEPES- or MES-buffered NaCl solution. The weight of bacterial cells in suspension was determined on a dry basis. Therefore, cell concentrations are shown in the unit of dry

TE

D

weight mg/ml below.

CE P

2.3. Dissolution of Fe-Mn nodule

2.3.1. Reductive dissolution of Fe and Mn

AC

20 mM HEPES- or MES-buffered NaCl solution and bacterial cell suspension were placed in a glass vessel. The Fe-Mn nodule sample was ground to a powder finer than 125 μm to achieve better leaching efficiency (Lee et al., 2001). The powdered Fe-Mn nodule (electron acceptor) and sodium lactate (electron donor) were added to the cell suspension. Mineral salts were also added to the solution in the following concentrations: 2.5 mM NH4Cl, 1.2 mM KCl, 1.1 mM MgSO4·7H2O, 0.61 mM CaCl2·2H2O, and 0.44 mM glycerophosphoric acid disodium salt. The vessel was incubated at 30°C in an anaerobic chamber, where the atmosphere was purged with Ar (95%) and H2 (5%) to maintain anaerobic conditions. A portion of solution was collected and filtered with a 0.2 µm pore-size PTFE filter in the chamber after 1, 2, 4, 7, 7

ACCEPTED MANUSCRIPT

10, and 20 days. The samples were acidified with 68% HNO3, and the Fe and Mn

T

concentrations were measured by inductively coupled plasma (ICP)-optical emission

IP

spectroscopy (OES) (iCAP 6300, Thermo Scientific, Waltham, MA). Divalent Fe and

SC R

Mn are water-soluble, whereas Fe(III) and Mn(IV) are insoluble. Thus, the reductive dissolution of Fe(III) and Mn(IV) was evaluated by using the dissolution rate defined as the ratio of amount in solution to total amount originally contained in the Fe-Mn nodule

NU

D535 sample (Table 1) as

(%)

(1).

MA

Dissolution rate = (Fe or Mn in solution)/(Fe or Mn in nodule) × 100

2.3.2. Adsorption rate of REEs on bacterial cells

TE

D

It was expected that REEs and other elements in the Fe-Mn nodule would be re-adsorbed on bacterial cells during the decomposition of the Fe-Mn nodule. Therefore,

CE P

bacterial cells were collected on a 0.2 µm pore-size PTFE filter, and decomposed with 34% HNO3 in a Teflon container on a hotplate at 180°C. REE concentrations in the

AC

decomposition solution and the filtered solution were determined by ICP-mass spectrometry (MS) (Agilent 7700, Agilent, Santa Clara, CA). Indium and Bi were added to be 1 ppb as internal standards in sample and standard solutions. The adsorption rate of REEs was defined as the ratio of amount adsorbed on bacterial cells to that originally contained in the Fe-Mn nodule as Adsorption rate = (REE on bacterial cell)/(REE originally contained in nodule) × 100

(%)

(2).

Cobalt, Ni, Cu, Zn, and Pb were also measured with a method similar to that for the REEs because they were enriched in Fe-Mn nodules useful metal resources (Table 1). The amounts of Fe and Mn remaining in the solid phase were measured using ICP-OES. 8

ACCEPTED MANUSCRIPT

T

2.3.3. Recovery of REEs from bacterial cells

IP

We examined the separation of REEs and other elements from the bacterial cells.

SC R

After dissolving the Fe-Mn nodule, the bacterial cells were collected on a 0.2 µm pore-size PTFE filter. The cells were rinsed with pure water (5 mL), and then leached with 0.01 M HCl (5 mL) three times. REEs, Co, Ni, Cu, Zn, and Pb in the rinse water

NU

and HCl leaching solutions were measured by ICP-MS. The desorption rate was defined

MA

as the ratio of the amount of desorbed elements to the amount adsorbed on bacterial cells as Desorption rate =

(%)

(3).

TE

D

(desorbed REE)/(REE initially adsorbed on bacterial cell) × 100

CE P

3. Results and discussion

3.1. Dissolution of Fe-Mn nodule

AC

We dissolved the Fe-Mn nodule in 0.01 and 0.1 M NaCl solutions with pH 7 at an initial concentration of 1.75 mM sodium lactate (70 μmol in 40 mL solution). The initial concentrations of bacterial cells and Fe-Mn nodule were 0.086 and 0.125 mg/mL (5 mg in 40 mL), respectively. The dissolution rate of Mn increased with time, and reached nearly 20% after 20 days (Fig. 2). However, Fe did not show significant amounts of dissolution over 20 days. The dissolution rates of Mn and Fe showed similar time-course variation in 0.01 and 0.1 M NaCl solutions although the rate for Mn was slightly higher in 0.1 M NaCl solution. The low dissolution rates indicated that the Fe-Mn nodule was not completely decomposed. The Fe-Mn nodule powder was visible even after 20 days. The reduction of Fe(III) and Mn(IV) by lactate occurs via the 9

ACCEPTED MANUSCRIPT

following reactions (Lovley et al., 1989): Lactate- + 2H2O + 4Fe3+ = Acetate- + HCO3- + 5H+ + 4Fe2+

T

(4) (5).

IP

Lactate- + H+ + HCO3- + 2MnO2 = Acetate- + 2H2O + 2MnCO3

SC R

The Fe and Mn concentrations in Fe-Mn nodule D535 were 12.7 and 12.8 wt%, respectively (Table 1). If reductive dissolution of the Fe-Mn nodule proceeded stoichiometrically according to reactions (4) and (5), 8.7 μmol of lactate would be

NU

required to decompose 5 mg Fe-Mn nodule powder completely. Therefore, the initial

MA

amount of sodium lactate (70 μmol) was sufficient to decompose the Fe-Mn nodule powder. However, lactate may have been consumed by cell growth in addition to Mn(IV) and Fe(III) reduction.

TE

D

Figure 2 shows that a larger amount of sodium lactate was necessary to decompose the Fe-Mn nodule powder completely. Therefore, we conducted further experiments

CE P

under the same conditions but with daily addition of sodium lactate. Every day, 70 μmol of sodium lactate was added to the solution, and the dissolution rate of Mn increased to

AC

~50% in 0.1 M NaCl solution, whereas Fe still showed a very low dissolution rate (Fig. 3). The dissolution rate was not improved in 0.01 M NaCl solution. The higher dissolution rate in 0.1 M NaCl solution suggests that the activity of S. putrefaciens was higher in solutions with higher NaCl concentrations. The daily addition of sodium lactate increased the dissolution rate of Mn in 0.1 M NaCl solution, although complete decomposition was not achieved (Fig. 3). We conducted further experiments, where the amounts of daily addition of sodium lactate were 0.07, 0.2, 0.5, 1 and 2 mmol per day, to examine the dependence of the dissolution of the Fe-Mn nodule on the amounts of sodium lactate. The dissolution rates of Mn and Fe increased as the amount of sodium lactate increased (Fig. 4). The Mn dissolution 10

ACCEPTED MANUSCRIPT

rates reached nearly 100% after 7 days in the solution with the daily addition of 1 and 2

T

mmol sodium lactate. The dissolution rates of Fe were around 80% after 10 days in the

IP

experiments with daily addition of 1 and 2 mmol sodium lactate. The dissolution rate of

SC R

Mn increased first, and then that of Fe increased, indicating that Mn(IV) was more readily reduced than Fe(III) (Figs 2, 3, and 4). This trend is reasonable because the Mn2+/MnO2 couple has a higher redox potential than the Fe2+/Fe(OH)3 couple (Brookins,

NU

1988). The dissolution rate of Fe did not reach 100% after 10 days, although the dark

MA

brown powders of the Fe-Mn nodule were no longer visible (Fig. S1, supplementary information). Furthermore, we analyzed Mn and Fe in the solid phases (bacterial cells and Fe-Mn nodule residue) after 20 days, but significant amounts of Mn and Fe were

TE

D

not detected. Therefore, we considered that Fe-Mn nodule was completely decomposed after 10 days. We obtained a similar result with 0.5 M NaCl solution with daily addition

CE P

of 1 mmol sodium lactate (Fig. 4).

Reductive dissolution of the Fe-Mn nodule in the presence of sodium lactate was

AC

observed even without adding the Fe-reducing bacteria (Fig. S2, supplementary information). However, the dissolution rates of Mn and Fe were much higher in the presence of bacteria, and did not reach 100% in the absence of bacteria. Therefore, the dissolution experiments demonstrated that microbial activity promoted the complete reductive dissolution of the Fe-Mn nodule (Lovley et al., 1989; Dollhopf et al., 2000; Lee et al., 2001).

3.2. Adsorption of REEs released from the Fe-Mn nodule Adsorption rates of REEs obtained from dissolution experiments are shown in Fig. 5. The adsorption rate of La reached the highest value of 40% (average of triplicate 11

ACCEPTED MANUSCRIPT

experiments) in 0.1 M NaCl solution with daily addition of 1 mmol sodium lactate. The

T

adsorption rate of REEs decreased with increasing atomic number from 40% to 15%.

IP

However, the adsorption rate ranged from 10 to 20% in 0.1 M NaCl solution with 2

SC R

mmol of the daily addition. The adsorption rates of light REEs decreased by about 20% in experiments with daily addition of 2 mmol sodium lactate compared with that of 1 mmol sodium lactate. It is possible that a portion of the added sodium lactate was not

NU

consumed by S. putrefaciens, and that REEs released from Fe-Mn nodule formed

MA

complexes with the remaining lactate in the solution (Deelstra and Verbeek, 1964). The formation of REE-lactate complexes could lower the adsorption rates to a larger degree in the experiment with daily addition of 2 mmol sodium lactate. Considering the

TE

D

adsorption rates of REEs, daily addition of 1 mmol sodium lactate was better for recovering REEs from Fe-Mn nodules.

CE P

The adsorption rates of REEs were higher in 0.5 M NaCl solution than in 0.1 M NaCl solution (Fig. 5). Other metallic elements contained in the Fe-Mn nodule could

AC

compete with REEs in adsorption on bacterial cells. The formation of chloride complexes may have decreased adsorption of other elements on the surface of bacteria, resulting in an increase in the adsorption rates of REEs. The adsorption rates of light REEs increased by 20-30% with increasing NaCl concentration, whereas those of heavy REEs increased by about 5% (Fig. 5). REEs form the stable carbonate complexes, REECO3+(aq) and REE(CO3)2-(aq), and their complexation constants increase with atomic number (Liu and Byrne, 1998; Ohta and Kawabe, 2000). Microbial activity produced carbon dioxide during reductive dissolution of the Fe-Mn nodule according to reactions (4) and (5). Therefore, it is possible that the formation of the REE carbonate complexes stabilized heavy REEs 12

ACCEPTED MANUSCRIPT

more and inhibited their adsorption on bacteria (Fig. 4).

T

Complexation of REEs with ligands would stabilize REEs in solution, resulting in

IP

less adsorption on the surface of bacteria. Lowering the solution pH was expected to

SC R

suppress the formation of carbonate and lactate complexes. Thus, we also conducted experiments at pH 5.5, 6, and 6.5 in 0.5 M NaCl solution with daily addition of 1 mmol sodium lactate to improve adsorption rates of heavy REEs. Complete dissolution of the

NU

Fe-Mn nodule was achieved at 5.5, 6, and 6.5 (data not shown). The adsorption rates of

MA

REEs decreased with decreasing pH (Fig. 6), and pH 7 was optimal for REEs to be adsorbed on bacteria under the experimental conditions studied here. We measured REEs remaining in solution at pH 7 after separation from bacterial cells. The percentage

TE

D

of the REEs not adsorbed on bacterial cells increased with atomic number from 5% to

bacterial cells.

CE P

70% (Fig. S3), which is a complement to the preferential adsorption of light REEs on

Of the conditions studied here, the best REE adsorption rates were obtained using

AC

0.5 M NaCl solution at pH 7 with daily addition of 1 mmol sodium lactate (Figs 5 and 6). The adsorption rates demonstrated that REEs released from the Fe-Mn nodule were adsorbed on bacterial cells, although heavy REEs showed low adsorption rates.

3.3. Adsorption of other elements Various metallic elements other than REEs are enriched in Fe-Mn nodules and crusts (Hein et al., 2003). The Fe-Mn nodule D535 contained Co, Ni, Cu, Zn, and Pb in high concentrations (Table 1). Therefore, we also examined the adsorption of these elements on bacterial cells. In 0.5 M NaCl solution at pH 7, the average adsorption rates obtained from triplicate experiments were nearly 100% for Cu and Pb, and about 80% 13

ACCEPTED MANUSCRIPT

for Zn (Fig. 7). In contrast, adsorption rates of Co and Ni were very low, although the

T

absolute amounts of adsorbed Co and Ni were much higher than those of REEs (Co:

IP

0.34 µg, Ni: 0.38 µg, Lu: 0.0053 µg). These elements may have occupied the limited

SC R

number of adsorption site on cell surfaces, which could result in competition between REEs and the other elements.

The low adsorption rate of Co indicates that most of the released Co was dissolved

NU

in solution (Fig. 7). In particular, Co is considered to be incorporated in Fe-Mn nodules

MA

as trivalent state (Dillard et al., 1982; Takahashi et al., 2007). Because Co(III) is insoluble, the dissolution of Co indicates that Co(III) was reduced to Co(II) during reductive dissolution of the Fe-Mn nodule. Similarly, Ce is tetravalent in the Fe-Mn

TE

D

nodule, D535 (Takahashi et al., 2007), and therefore Ce(IV) would have been reduced to Ce(III). If Ce(IV) had not been reduced to Ce(III), the adsorption rate of Ce would be

CE P

deviated largely from those of the neighboring REEs, i.e. La and Pr (Figs 5 and 6). In addition, the dissolved fraction of Ce in solution supports the reduction of Ce(IV) (Fig.

AC

S3). Dissolution experiments showed the reductive dissolution of Fe(III) in the Fe-Mn nodule (Fig. 4). The reduction of Co(III) and Ce(IV) is reasonable, considering that the redox potentials of Co2+/CoOOH and Ce3+/CeO2 couples are higher than the Fe2+/Fe(OH)3 couple (Brookins, 1988).

3.4. Recovery and separation of REEs adsorbed on bacteria cells The REEs and other elements were adsorbed on bacterial cells after dissolution of the Fe-Mn nodule (Figs 5, 6, and 7). We examined the recovery of REEs adsorbed on bacterial cells and their separation from other elements (Fig. 8). A substantial amount of REEs was not desorbed by rinsing the bacterial cells with pure water (Fig. 8a). During 14

ACCEPTED MANUSCRIPT

the first addition of 0.01 M HCl, 40% to 50% of the REEs were desorbed. The

T

desorption amounts of the REEs decreased during the second and third addition. Finally,

IP

70 – 80% of the REEs were recovered from bacterial cells by adding 0.01 M HCl three

SC R

times. However, 10% of Zn and 20% of Co and Ni were desorbed by rinsing with pure water, suggesting that these elements were weakly adsorbed (Fig. 8b). The subsequent addition of 0.01 M HCl could leach the remaining amounts of these elements from the

NU

bacterial cells. The low adsorption rates of Co and Ni and the high desorption rates

MA

indicate that these elements were partly separated from REEs during the dissolution of the Fe-Mn nodule and re-adsorption on bacterial cells (Figs 6 and 7). Half the amount of Pb was desorbed by the triplicate additions of 0.01 M HCl. Only 10% of Cu was

TE

D

desorbed from bacterial cells. It is possible that Cu was not only adsorbed on cell surfaces but also incorporated into cells (Navarrete et al., 2011). The low desorption rate

CE P

indicated that Cu could be separated well from REEs (Fig. 8). Bioleaching of metal sulfides has been extensively investigated with Fe-oxidizing

AC

bacteria (Sand et al., 2001; Tributsch, 2001; Vera et al., 2013). However, REE abundances are very low in sulfides compared with Fe-Mn nodules and crusts (Terakado and Walker, 2005). Therefore, using Fe-Mn nodules and crusts is a promising way to ensure a variety of REE resources. In this study, we demonstrated that decomposition of Fe-Mn oxide and recovery of REEs can be achieved simultaneously in a single solution system by using Fe-reducing bacteria (Figs 4, 5 and 6). This method is an environmentally friendly method and can decrease the amount of acids used in chemical processing of Fe-Mn nodules and crusts.

4. Conclusions 15

ACCEPTED MANUSCRIPT

We dissolved Fe-Mn nodule powder in NaCl solution using S. putrefaciens. The

T

Fe-Mn nodule was decomposed with daily addition of sodium lactate as an electron

IP

donor. The adsorption amounts of REEs on the bacterial cells after their release from the

SC R

Fe-Mn nodule depended on the amount of sodium lactate and pH because of the complexation of REEs with sodium lactate and with carbonate produced by bacterial activity. Of the conditions studied here, the best adsorption rates of REEs were obtained

NU

by using 0.5 M NaCl solution at pH 7 with daily addition of 1 mmol sodium lactate.

MA

Most REEs adsorbed on the bacterial cells could be recovered by leaching with 0.01 M HCl. The reductive dissolution of Fe-Mn nodules using Fe-reducing bacteria is a promising environmentally friendly method for recovery of REEs as well as other

CE P

Acknowledgements

TE

D

metallic elements from Fe-Mn nodules and crusts.

This research did not receive any specific grant from funding agencies in the public,

AC

commercial, or not-for-profit sectors. The authors appreciate constructive comments by two anonymous reviewers.

16

ACCEPTED MANUSCRIPT

References

T

Bau M, Koschinsky A, Dulski P, Hein JR (1996) Comparison of the partitioning

IP

behaviours of yttrium, rare earth elements, and titanium between hydrogenetic

SC R

marine ferromanganese crusts and seawater. Geochim Cosmochim Acta. 60:1709-1725. doi:10.1016/0016-7037(96)00063-4

Brookins DG (1988) Eh–pH Diagrams for Geochemistry. Springer-Verlag, Berlin.

NU

De Carlo EH, McMurtry GM (1992) Rare-earth element geochemistry of

MA

ferromanganese crusts from Hawaiian Archipelago, central Pacific. Chem Geol 95:235-250. doi:10.1016/0009-2541(92)90014-V Deelstra H, Verbeek F (1964) The determination of the stability constants of the

TE

D

lanthanide α-hydroxyisobutyrate and lactate complexes by potentiometric titration. Anal. Chim. Acta 31:251-257. doi:10.1016/S0003-2670(00)88816-9

CE P

Dillard JG, Crowther DL, Murray JW (1982) The oxidation states of cobalt and selected metals in Pacific ferromanganese nodules. Geochim Cosmochim Acta 46:755-759.

AC

doi:10.1016/0016-7037(82)90027-8 Dollhopf ME, Nealson KH, Simon DM, Luther GW III (2000) Kinetics of Fe(III) and Mn(IV) reduction by the Black Sea strain of Shewanella putrefaciens using in situ solid

state

voltammetric

Au/Hg

electrodes.

Mar

Chem

70:171-180.

doi:10.1016/S0304-4203(00)00021-9 Dymond J, Lyle M, Finney B, Piper DZ, Murphy K, Conard R, Pisias N (1984) Ferromanganese nodules from MANOP Sites H, S, and R—control of mineralogical and chemical composition by multiple accretionary processes. Geochim Cosmochim Acta 48:931-949. doi:10.1016/0016-7037(84)90186-8 Eliseeva SV, Bünzli J-CG (2011) Rare earths: jewels for functional materials of the 17

ACCEPTED MANUSCRIPT

future. New J Chem 35:1165-1176. doi:10.1039/c0nj00969e

T

Gupta CK, Krishnamurthy N (2004) Extractive Metallurgy of Rare Earths. CRC Press,

IP

Boca Raton.

SC R

Hein JR, Koschinsky A, Halliday AN (2003) Global occurrence of tellurium-rich ferromanganese crusts and a model for the enrichment of tellurium. Geochim Cosmochim Acta 67:1117-1127. doi:10.1016/S0016-7037(00)01279-6

NU

Hein, JR, Mizell, K., Koschinsky, A., Conrad, T.A. (2013) Deep-ocean mineral deposits

MA

as a source of critical metals for high- and green-technology applications: Comparison with land-based resources. Ore Geology Reviews 51:1-14. doi: 10.1016/j.oregeorev.2012.12.001

TE

D

Kanazawa Y, Kamitani M (2006) Rare earth minerals and resources in the world. J. Alloys Compd 408-412:1339-1343. doi:10.1016/j.jallcom.2005.04.033

CE P

Lee EY, Noh SR, Cho KS, Ryu HW (2001) Leaching of Mn, Co, and Ni from manganese nodules using an anaerobic bioleaching method. J Biosci Bioeng

AC

92:354-359. doi:10.1016/S1389-1723(01)80239-5 Liu X, Byrne RH (1998) Comprehensive investigation of yttrium and rare earth element complexation by carbonate ions using ICP-Mass spectrometry. J Sol Chem 27:803-815. Lovley DR, Phillips EJP, Lonergan DJ (1989) Hydrogen and formate oxidation coupled to dissimilatory reduction of iron or manganese by Alteromonas putrefaciens. Appl Environ Microbiol 55:700-706. Mariano AN, Mariano A (2013) Rare earth mining and exploration in North America. Elements 8:369-376. doi: 10.2113/gselements.8.5.369 Navarrete JU, Borrok DM, Viveros M, Ellzey JT (2011) Copper isotope fractionation 18

ACCEPTED MANUSCRIPT

during surface adsorption and intracellular incorporation by bacteria. Geochim

T

Cosmochim Acta 75:784-799. doi:10.1016/j.gca.2010.11.011

IP

Ohta A, Kawabe I (2000) Rare earth element partitioning between Fe oxyhydroxide

SC R

precipitates and aqueous NaCl solutions doped with NaHCO3: Determinations of rare earth element complexation constants with carbonate ions. Geochem J 34:439-454.

NU

Ohta A, Kawabe I (2001) REE(III) adsorption onto Mn dioxide (δ-MnO2) and Fe

MA

oxyhydroxide: Ce(III) oxidation by δ-MnO2. Geochim Cosmochim Acta 65:695-703.

Ohta A, Ishii S, Sakakibara M, Mizuno A, Kawabe I (1999) Systematic correlation of

TE

D

the Ce anomaly with the Co/(Ni+Cu) ratio and Y fractionation from Ho in distinct types of Pacific deep-sea nodules. Geochem J 33:399-417.

CE P

Piepgras DJ, Jacobsen SB (1992) The behavior of rare earth elements in seawater: Precise determination of variations in the North Pacific water column. Geochim

AC

Cosmochim Acta 56:1851-1862. doi: 10.1016/0016-7037(92)90315-A Sand W, Gehrke T, Jozsa P-G, Schippers A (2001) (Bio) chemistry of bacterial leaching—direct

vs.

indirect

bioleaching.

Hydrometallurgy

59:159-175.

doi:10.1016/S0304-386X(00)00180-8 Suzuki Y, Sakama Y, Saiki H, Kitamura A, Yoshikawa H, Tanaka K (2014) Immobilization of selenium by biofilm of Shewanella putrefaciens with and without Fe(III)-citrate

complex.

J

Nucl

Sci

Technol

51:108-115.

doi:

10.1080/00223131.2013.851041 Takahashi Y, Châtellier X, Hattori HK, Kato K, Fortin D (2005) Adsorption of rare earth elements onto bacterial cell walls and its implication for REE sorption onto natural 19

ACCEPTED MANUSCRIPT

microbial mats. Chem Geol 219:53-67. doi:10.1016/j.chemgeo.2005.02.009

T

Takahashi Y, Manceau A, Geoffroy N, Marcus MA, Usui A (2007) Chemical and

IP

structural control of the partitioning of Co, Ce, and Pb in marine ferromanganese

SC R

oxides. Geochim Cosmochim Acta 71:984-1008. doi:10.1016/j.gca.2006.11.016 Takahashi Y, Yamamoto M, Yamamoto Y, Tanaka K (2010) EXAFS study on the cause of enrichment of heavy REEs on bacterial cell surfaces. Geochim Cosmochim

NU

Acta 74:5443-5462. doi:10.1016/j.gca.2010.07.001

MA

Terakado Y, Walker RJ (2005) Nd, Sr and Pb isotopic and REE geochemical study of some Miocene submarine hydrothermal deposits (Kuroko deposits) in Japan. Contrib Mineral Petrol 149:388-399. doi:10.1007/s00410-005-0661-z

TE

D

Tributsch H (2001) Direct versus indirect bioleaching. Hydrometallurgy 59:177-185. doi:10.1016/S0304-386X(00)00181-X

CE P

Usui A, Nohara M, Okubo Y, Nishimura A, Yamazaki T, Saito Y, Miyazaki J, Tsurusaki K, Yamazaki T, Harada K, Lee CW, Fleming P (1994) Outline of the

AC

cruise GH83-3 in the penrhyn basin, south pacific. Geological survey of Japan Cruise Report 23:1-17.

Vera M, Schippers A, Sand W (2013) Progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation—part A. Appl Microbiol Biotechnol 97:7529-7541. doi:10.1007/s00253-013-4954-2 Wu C-Y, Huang D-H, Guo Z-X (1990) REE geochemistry in the weathered crust of granites, Longnan area, Jiangxi Province. Acta Geol Sinica 64:193-210. Zhang J, Nozaki Y (1996) Rare earth elements and yttrium in seawater: ICP-MS determinations in the East Caroline, Coral Sea, and South Fiji basins of the western South

Pacific

Ocean.

Geochim 20

Cosmochim

Acta

60:4631-4644.

ACCEPTED MANUSCRIPT

AC

CE P

TE

D

MA

NU

SC R

IP

T

doi:10.1016/S0016-7037(96)00276-1

21

ACCEPTED MANUSCRIPT

Figure captions

T

Fig. 1 Flow diagram showing experimental steps.

IP

Fig. 2 Time-course dissolution of Mn and Fe by S. putrefaciens in 0.01 and 0.1 M NaCl

SC R

solutions at pH 7. The initial concentrations of bacterial cells and Fe-Mn nodule were 0.086 and 0.125 mg/mL, respectively. Sodium lactate was added as an electron acceptor at the initial concentration of 1.75 mM (70 μmol in 40 mL)

NU

Fig. 3 Time-course dissolution of Mn and Fe by S. putrefaciens in 0.01 and 0.1 M NaCl

MA

solutions at pH 7. The initial concentrations of bacterial cells and Fe-Mn nodule were 0.086 and 0.125 mg/mL, respectively. Every day, 70 μmol of sodium lactate was added as an electron acceptor

TE

D

Fig. 4 Time-course dissolution of (a) Mn and (b) Fe by S. putrefaciens in 0.1 M NaCl solution at pH 7. The initial concentrations of bacterial cells and Fe-Mn nodule

CE P

were 0.073 and 0.125 mg/mL, respectively. The amount of sodium lactate added daily is indicated in the figure legends

AC

Fig. 5 Adsorption rates of REEs in 0.1 or 0.5 M NaCl solution at pH 7. Dissolution experiments were conducted with daily addition of 1 and 2 mmol sodium lactate. The initial concentrations of the Fe-Mn nodule and bacterial cells were 0.125 and 0.073 mg/mL, respectively. Error bars indicate standard deviations of the triplicate experiments Fig. 6 Adsorption rates of REEs in 0.5 M NaCl solutions under different pH conditions. Dissolution experiments were conducted with daily addition of 1 mmol sodium lactate. The initial concentrations of the Fe-Mn nodule and bacterial cells were 0.125 and 0.1 mg/mL, respectively. Error bars indicate standard deviations of the triplicate experiments 22

ACCEPTED MANUSCRIPT

Fig. 7 Adsorption rates of Co, Ni, Cu, Zn, and Pb in 0.5 M NaCl solution at pH 7.

T

Triplicate dissolution experiments were conducted with daily addition of 1 mmol

IP

sodium lactate. The initial concentrations of the Fe-Mn nodule and bacterial cells

SC R

were 0.125 and 0.1 mg/mL, respectively

Fig. 8 Desorption of (a) REEs and (b) Co, Ni, Cu, Zn, and Pb from bacterial cells by leaching with 0.01 M HCl. Dissolution experiments were conducted in 0.5 M NaCl

NU

solution at pH 7 with daily addition of 1 mmol sodium lactate. The initial

MA

concentrations of the Fe-Mn nodule and bacterial cells were 0.125 and 0.1 mg/mL,

AC

CE P

TE

D

respectively

23

ACCEPTED MANUSCRIPT

Fe (wt%) 12.7

Co (ppm) 4750

Cu (ppm) 1020

Ni (ppm) 2820

Zn (ppm) 465

Pb (ppm) 714

La (ppm) 177

Ce (ppm) 1230

Pr (ppm) 41.3

Nd (ppm) 164

Sm (ppm) 38.3

Eu (ppm) 8.97

Gd (ppm) 40.3

Tb (ppm) Dy (ppm) Ho (ppm) 5.9 33.8 6.89 a Data from Takahashi et al. (2007)

Er (ppm) 20.2

Tm (ppm) 2.88

Yb (ppm) 19.3

Lu (ppm) 2.95

SC R

NU MA D TE CE P AC

24

T

Mn (wt%) 12.8

IP

Table 1. Chemical composition of the Fe-Mn nodule, D535.a

Y (ppm) 130

CE P

AC

Figure 1

TE

D

MA

NU

SC R

IP

T

ACCEPTED MANUSCRIPT

25

AC

CE P

TE

D

MA

NU

SC R

IP

T

ACCEPTED MANUSCRIPT

Figure 2

26

AC

CE P

TE

D

MA

NU

SC R

IP

T

ACCEPTED MANUSCRIPT

Figure 3

27

MA

NU

SC R

IP

T

ACCEPTED MANUSCRIPT

AC

CE P

TE

D

Figure 4

28

AC

CE P

TE

D

MA

NU

SC R

IP

T

ACCEPTED MANUSCRIPT

Figure 5

29

AC

CE P

TE

D

MA

NU

SC R

IP

T

ACCEPTED MANUSCRIPT

Figure 6

30

AC

CE P

TE

D

MA

NU

SC R

IP

T

ACCEPTED MANUSCRIPT

Figure 7

31

MA

NU

SC R

IP

T

ACCEPTED MANUSCRIPT

AC

CE P

TE

D

Figure 8

32

ACCEPTED MANUSCRIPT

AC

CE P

TE

D

MA

NU

SC R

IP

T

Highlights • Fe-Mn nodule powder was reductively decomposed by using Fe-reducing bacterium. • REEs released from the Fe-Mn nodule were adsorbed on bacterial cells. • Most of the adsorbed REEs were recovered by leaching with 0.01 M HCl.

33