Next Article in Journal
Childhood Trauma and Psychological Distress: A Serial Mediation Model among Chinese Adolescents
Previous Article in Journal
Concentrations of Seven Phthalate Monoesters in Infants and Toddlers Quantified in Urine Extracted from Diapers
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
IJERPH
Volume 18
Issue 13
10.3390/ijerph18136807
ijerph-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Insight to Microbial Fe(III) Reduction Mediated by Redox-Active Humic Acids with Varied Redox Potentials

by
Jingtao Duan
1,
Zhiyuan Xu
1,
Zhen Yang
2 and
Jie Jiang
1,*
1
College of Environmental Science and Engineering, Beijing Forestry University, Beijing 100083, China
2
College of Urban and Environmental Science, Peking University, Beijing 100871, China
*
Author to whom correspondence should be addressed.
Int. J. Environ. Res. Public Health 2021, 18(13), 6807; https://doi.org/10.3390/ijerph18136807
Submission received: 2 June 2021 / Revised: 20 June 2021 / Accepted: 21 June 2021 / Published: 24 June 2021
(This article belongs to the Section Environmental Science and Engineering)
Browse Figures
Versions Notes

Abstract

:
Redox-active humic acids (HA) are ubiquitous in terrestrial and aquatic systems and are involved in numerous electron transfer reactions affecting biogeochemical processes and fates of pollutants in soil environments. Redox-active contaminants are trapped in soil micropores (<2 nm) that have limited access to microbes and HA. Therefore, the contaminants whose molecular structure and properties are not damaged accumulate in the soil micropores and become potential pollution sources. Electron transfer capacities (ETC) of HA reflecting redox activities of low molecular weight fraction (LMWF, <2.5) HA can be detected by an electrochemical method, which is related to redox potentials (Eh) in soil and aquatic environments. Nevertheless, electron accepting capacities (EAC) and electron donating capacities (EDC) of these LMWF HA at different Eh are still unknown. EDC and EAC of different molecular weight HA at different Eh were analyzed using electrochemical methods. EAC of LMWF at −0.59 V was 12 times higher than that at −0.49 V, while EAC increased to 2.6 times when the Eh decreased from −0.59 V to −0.69 V. Afterward, LMWF can act as a shuttle to stimulate microbial Fe(III) reduction processes in microbial reduction experiments. Additionally, EAC by electrochemical analysis at a range of −0.49–−0.59 V was comparable to total calculated ETC of different molecular weight fractions of HA by microbial reduction. Therefore, it is indicated that redox-active functional groups that can be reduced at Eh range of −0.49–−0.59 are available to microbial reduction. This finding contributes to a novel perspective in the protection and remediation of the groundwater environment in the biogeochemistry process.

1. Introduction

Humic acids (HA) as redox-active organic compounds can directly or indirectly affect the fates of pollutants in soil and water environments [1,2,3,4]. HA can reduce Mn(IV) and Hg(II) via serving as an electron donor in soils and sediments and thus play a role in the abiotic dark reduction in waters, sediments, and soils [4,5,6]. HA are supramolecular compounds of diverse self-assembled low molecular mass organic molecules, which form dynamic associations linked through hydrogen bridges and hydrophobic bonds [7,8,9]. Low molecular weight fraction (LMWF) of HA can be isolated by a new membrane dialysis method, and they can flow into soil micropores where many redox-active pollutants are trapped [10]. LMWF HA provides the possibility of bioremediation to treat active-redox contaminants in soil micropores.
Redox activities of HA are associated with the number of redox-active functional groups (RAFGs) and redox potentials (Eh). HA possess electron accepting capacities (EAC) and electron donating capacities (EDC) depending on the state of RAFGs [1,11,12] including electron donating groups [13,14,15] and electron accepting groups [16,17,18]. Studies have shown that RAFGs of humus varies at different Eh. At pH 7, the distribution range of Eh is −200–+300 mV [19]. Many studies have expanded the range of oxidation state potential distribution from +320 mV to +700 mV [20], and to +778 mV (pH = 5) [21]. Peat soil HA can be reduced and oxidized in a wide varied Eh range of −0.9 to +1.0 V by electrochemical methods [2]. By using direct electrochemical reduction/oxidation of HA at a glassy carbon working electrode, the monitored time–current curve at different Eh can be obtained and the EAC and EDC can be accurately calculated [1]. Although strong redox capacities of LMWF HA have been demonstrated by chemical reduction analysis [10], it has not been clarified the availability of Eh range at which that EAC and EDC of LMWF HA can be detected, and to what extent of EDC of LMWF HA at specific Eh by this novel electrochemical method.
Ferrous iron compounds/minerals are able to function as reductants for organic and inorganic contaminants including nitro benzenes, arsenic, and selenium [1,22,23,24]. Fe(III)-oxyhydroxides and Fe(III)-bearing clay minerals (e.g., ferrihydrite (Fh)) predominantly occurs as poorly soluble forms in natural environments [25]. Thus, the microbially mediated iron reduction can only be achieved by transferring electrons extracellularly as insoluble Fe(III) minerals cannot diffuse into the interior of the dissimilatory iron-reducing prokaryotes (e.g., Shewanella spp.). The extracellular electron transfer (EET) pathways, including HA function as an electron shuttle, are developed to mediate electrons’ transfer between microbes and poorly soluble Fe(III) minerals [26,27,28]. Microbes can donate electrons to native HA and then reduce HA flow into and/or out of the soil micropores to change the fate of redox-active minerals (i.e., iron) or contaminants [29,30]. Electron shuttle capacities (ESC) of HA [2,31,32,33] and the microbial EET pathways are highly dependent on cell membrane potential [34,35,36,37]. Until now, whether LMWF HA could act as an electron shuttle to stimulate microbial Fe(III) reduction under available Eh range, and the differences and link of ETC between electrochemical and microbial reduction has not been fully studied.
To this end, we collected different molecular weight fractions (LMWF and retentate) using a dialysis method, with the pore size diameter of 1.25 nm and 2.5 nm as in the previous study [10]. Subsequently, the aims of this study were (i) to determine electron exchange capacity (EEC), including electron EAC and EDC of LMWF, retentate, and bulk HA at a varied Eh range of −0.49 to −0.69 V using electrochemical analysis; (ii) to determine ESC of LMWF, retentate, and bulk HA using microbial Fh reduction experiments in comparison to EEC by electrochemical analysis; and (iii) to develop a potential relationship between EEC by electrochemical method and ESC by microbial method. This study aims to provide a better understanding of the electron transfer process of HA during the biogeochemistry process thus predicting the potential fates of pollutants in soil and groundwater environments.

2. Materials and Methods

2.1. Preparation of HA Solution

0.25 g Leonardite humic acids Standard (LHA) and 0.25 g Pahokee peat humic acids Standard (PPHA), purchased from the International Humic Substances Society (IHSS), were dissolved with 50 mM phosphate buffer solution (PP buffer, pH = 7) respectively and reached a final concentration of 0.5 mg/mL. The HA samples were stored in blue-capped bottles covered with aluminum foil wrap and then stored in the fridge (4 °C) to inhibit the photochemical reaction.

2.2. Dialysis Experiment

Dialysis bags were purchased from MWCO Regenerate (VISKASE, US). MD34-3500 and MD34-14,000 with a pore size of 1.25 nm and 2.5 nm were chosen in this study. Cut out dialysis bags of a certain length were soaked in deionized water for 24 h before dialysis experiments to remove impurities from itself effectively. Fifty milliliters of bulk HA (0.5 mg/mL) was transferred accurately into the pretreated dialysis bag. After being sealed with dialysis clamps, it was put into a 400 mL beaker containing 200 mL buffer and then totally immersed. Before being put on a magnetic stirrer (IKA, Germany) constantly stirring (500 rpm) for 72 h, the beaker was sealed with a sealing film to avoid debris from entering and the whole device was wrapped with aluminum foil wrap to prevent a photochemical reaction. The molecular size that less than 3500 (or 14,000) dalton HA fractions would release into the solvent (PP buffer) during the dialysis process, which were named as LMWF, and those fractions that failed to be out of the dialysis bag were named as retentate. Total organic carbon (TOC) contents of bulk LHA, LMWF HA, and retentate HA were determined respectively by a TOC-Vcsn analyzer (SHIMADZU).

2.3. Electrochemical Analysis with Direct Electrochemical Reduction and Oxidation

All electrochemical experiments were conducted in an anoxic glove box (100% N2 atmosphere). A platinum disk working electrode (CHI102), a Pt wire counter electrode (CHI115), and an Ag/AgCl reference electrode (CHI111) (CH Instruments, Inc., Austin, TX, USA) composed of the electrolytic cell system. The current response I was determined by CH Instruments 660E (Austin, TX, USA). The supporting electrolyte was 0.1 M KCl during the electrochemical experiment. Each sample was direct electrochemical reduction at various electrode potentials of −0.49 V, −0.59 V, and −0.69 V, respectively, and was direct electrochemical oxidation at +0.61 V. EDC, EAC, and EEC (mmole-/g C) of different molecular weight HA samples were calculated and normalized to TOC as previously described by Xu et al. [12] as follow:
EDC = Q DEO TOC × V = ∫ I OX F dt TOC × V
EAC = Q DER TOC × V = ∫ I RE F dt TOC × V
QDER and QDEO (μmol) were the number of transferred electrons in direct electrochemical reduction/oxidation experiments, F is a Faraday constant (96,485 (C/mol)) and V(mL) is a volume of reaction samples.

2.4. Microbiological Analysis with Shewanella oneidensis MR-1 Fe(III) Reduction

Experiments were carried out under anaerobic conditions in the glove box (pH 7, 100% N2). The total volume of the reactor was 2 mL, in which the volume of Shewanella oneidensis MR-1 (OD = 1) was 200 μL, the concentration of Fh (the terminal electron acceptor) was 1 mmol/L, the volume of LMWF HA/retentate or bulk was 1000/100 μL, and the remaining part was filled up with Shewanella basal medium SBM containing lactate (the sole electron donor). Fh was prepared according to Cornell and Schwertmann [38], and the amount of Fe(II) was quantified as previously described by Stookey [39].
ESC is defined as the stimulation effect of HA on microbial Fe(III) reduction process. Numerically ESC is equal to the difference in the amount of Fe(II) (μmol) produced in the presence and absence (blank experiment) of HA samples in microbial Fe(III) reduction experiments. Considering different molecular weight fractions have different TOC contents, ESC (mmol e-/g C) of each sample was normalized to TOC.

3. Results and Discussion

3.1. Dialysis Experiment and TOC Contents

High-performance size-exclusion chromatography (HPSEC) is used in the past decades to isolate different molecular weights of HA [40], while we select the dialysis method to collect different molecular weight fractions of HA to better compare to the results of our previous studies. In this study, dialysis experiments were conducted within 3 days (72 h) to obtain different molecular weight HA fractions. The TOC contents of all samples were shown in Table 1. The results showed diversity in TOC between LMWF and bulk HA. 3500-LMWF of LHA and PPHA account for 2.0% and 3.6% of bulk HA, respectively, which were comparable to our previous study [10]. In contrast, retentate HA of all samples had similar TOC contents with the bulk HA. TOC contents of LMWF PPHA and bulk PPHA were higher than those of LHA, indicating that bulk PPHA was able to release more LMWF compared to bulk LHA during dialysis. TOC contents of 14,000-LMWF LHA (9.14 mg C/L) and 14,000-LMWF PPHA (11.62 mg C/L) were higher than 3500-LMWF LHA (4.61 mg C/L) and 3500-LMWF PPHA (8.48 mg C/L) (Table 1), which demonstrated that LMWF ranged from 3500–14,000 Dalton has a contribution to bulk HA TOC contents. In addition, the TOC of 3500-LMWF and 14,000-LMWF HA are in the range of concentrations that are common in terrestrial and aquatic environments including rivers, oceans, estuaries, and sediments [41,42,43,44,45,46] where the concentration of dissolved organic carbon ranges from 7 to 30 mg C/L in nature [47,48].

3.2. Direct Electrochemical Reduction/Oxidation of Different Molecular Weight Fractions of HA Samples

Electrochemical methods were used to investigate the contribution of LMWF, retentate, and bulk HA to EEC which is the sum of EAC and EDC. Direct electrochemical reduction/oxidation were used to monitor current I over the time t (s) of different molecules HA in Eh range of −0.69 V to +0.61 V by electrochemical analysis in this study. Direct electrochemical oxidation experiments were conducted at +0.61 V. Current I–t of LMWF, retentate, and bulk HA are showed in Figure 1. EDC at +0.61 V were calculated based on oxidative current I–t and were normalized to TOC contents (Figure 2). EDC was detected for all LMWF HA with −0.8 to −1.4 meq e−/g C, and retentate and bulk HA with −0.03 to −0.04 meq e−/g C. This result suggested that different molecular weight fractions of LHA and PPHA had different EDC. Compared to LMWF HA, retentate and bulk HA showed a lower EDC, which means LMWF is the main contributor in donating electrons.
Direct electrochemical reduction experiments were conducted under three Eh (−0.49 V; −0.59 V; −0.69 V). Current I–t and corresponding EAC are showed in Figure 3 and Figure 4, respectively. Current I–t results indicated a similar decreasing tendency of PPHA and LHA. In addition, the current I–t of all molecular fractions of both PPHA and LHA increased with a decreasing Eh from −0.49 V to −0.69 V, revealing that EAC of HA was highly related to environment Eh. Additionally, EAC at −0.59 V was 12 times more than that at −0.49 V, while EAC increased 2.6 times when the potential decreased from −0.59 V to −0.69 V. These results further declared that although EAC of HA was dependent on the Eh of the environment, the significant enhancement of EAC between −0.49 V and −0.59 V illustrated that there were many RAFGs in HA within this range of potential. EAC of different molecular weight fractions of PPHA and LHA increased with Eh decreasing. LMWF showed a remarkably higher EAC per gram of carbon compared to retentate and bulk HA, which was consistent with previous studies [10], indicating that LMWF had a larger number of RAFGs than bulk HA.
Direct electrochemical reduction and oxidation experiments (Figure 1 and Figure 3) and corresponding EDC and EAC (Figure 2 and Figure 4) of all different molecular weight LHA and PPHA illustrated that HA was able to act as redox buffers, which are in agreement with previous studies [2,49]. EAC and EDC of different molecular weight fractions had been normalized to the number of electrons transferred per gram carbon (meq e-/g C) to further compare EAC and EDC of different molecular weight LHA and PPHA. Results showed that EDC of LHA and PPHA were significantly smaller than their EAC (Figure 2 and Figure 4), indicating that native HA were easier to be reduced than to be oxidized.

3.3. ESC of Different Molecular Weight Fractions of HA Samples

LMWF HA showed a strong EAC by electrochemical reduction; however, whether LMWF HA can act as an electron shuttle to stimulate electron transfer in the microbial Fh reduction process is not clear. Therefore, microbial Fe(III) reduction experiments were conducted in the presence and absence of different molecular weight fractions of HA to clarify the stimulation effect. In the 2 mL reactor, LMWF, retentate, and bulk HA were reduced by Shewanella oneidensis MR-1, respectively, and then they could act as electron shuttles to accelerate microbial-Fh reduction processes. There was less Fe(II) formation in the presence of LMWF HA compared to those with retentate and bulk (Figure 5), indicating that the redox capabilities of different molecular weight fractions of HA were highly dependent on its TOC contents, which was consistent with our electrochemical results. Additionally, there was more Fe(II) formation when Fh was reduced by the microbial reduced HA compared to directly reduced by Shewanella oneidensis MR-1 (Figure 5), showing that all different molecular weight fraction HA can act as an electron shuttle to stimulate microbial-Fh reduction processes.
ESC of different molecular weight HA was normalized to its TOC contents (meq e-/g C) (Figure 6). LMWF LHA and PPHA were 3.8–8.5 and 3.0–3.7 times higher than that of the retentate and bulk LHA and PPHA respectively, which was in accordance with electrochemical results describing high EAC of LMWF HA. It has been proved that bulk HA can facilitate the reduction of iron(III) oxide in sediments and soils [50]. Our results further demonstrate that LMWF with high EAC can also act as an electron shuttle in the microbial Fe(III) reduction process. Additionally, microbial reduced LMWF HA maybe serve as a crucial electron shuttle to reduce pollutants (Hg(II), U(VI), and Cr(VI)) and convert them to less toxic forms or remove them [51], when those contaminates are occluded in tight pore spaces that microorganisms cannot enter, particularly.
EAC and ESC revealed electron transfer capacities (ETC) in different conditions. EAC reflected redox capability of different molecular weight HA at 3 specifics Eh values and ESC showed their capabilities in a changing Eh environment. HA may be reduced under varying redox conditions and the potential ranges of microbial reduction is −0.60 to 0.24 V [52]. In our study, the membrane potential of Shewanella oneidensis MR-1 would keep changing since the whole process is a dynamic system of continuous Fe(II) formation, which would then have an impact on the electron transfer both from microbial to HA and HA to Fh. For further comparison ETC of different molecular weight HA reduced electrochemically and microbially, ETC in the 2 mL reactors was calculated and showed in Table 2, per gram of carbon ETC are showed in Figure 7. The electron-carrying capacities of PPHA and LHA measured in an anaerobic chamber [53] were 0.87 meq/g C and 0.78 meq/g C, respectively, which are comparable with ETC of bulk PPHA and LHA in our study.
While PPHA showed a higher ETC than LHA when in 4 mL reactors (Table 2), LHA showed a higher ETC than PPHA when considering the effect of TOC, demonstrating that TOC had a significant influence when calculating ETC. Table 2 and Figure 7 showed that ETC of different molecular weight fractions of PPHA and LHA by microbial reduction was comparable to ETC by electrochemical analysis at a range of −0.49–−0.59 V whether considering per unit volume or per TOC, which suggests that an EET pathway can be achieved between Fe(III)-reducing bacteria (S. oneidensis MR-1) and native different molecular weight fractions of PPHA and LHA in the Eh range of −0.49–−0.59 V and this is comparable to the previous study [52].

4. Conclusions

Redox properties of HA, which are further pertinent to the fate of transformation and transport of redox-active contaminants in the environment, are highly dependent on the chemical composition and characteristics of HA such as Eh and RAFGs. The present study, for the first time, investigated the difference in ETC of LMWF, retentate, and bulk LHA and PPHA between microbial and electrochemical reduction. The results indicated that EAC of all molecular weight LHA and PPHA increased with a reduced Eh range from −0.49 V to −0.69 V. LMWF LHA and PPHA showed dramatic higher EAC compared to retentate and bulk LHA and PPHA. Microbial reduced LMWF LHA and PPHA also showed strong ESC, and their ETC was comparable to that reduced electrochemically in the Eh range of −0.49 to −0.59 V, which further illustrated that LMWF LHA and PPHA could act as an electron shuttle between Shewanella oneidensis MR-1 and Fh in this Eh condition. Our study provides a new perspective in the electron transfer processes via directed towards microbial and electrochemical research to identify redox-active HS in varied Eh soil conditions, which may link to predicate degradation and redox of pollutants trapped in soil micropores (<2 nm). LMWF HA can provide the direct or indirect interactions with pollutants (POPs, As, P, Hg, U, and Cr) trapped in soil micropore and then change the fate of the contaminate involved in microbial Fe(III) reduction processes.

Author Contributions

Conceptualization, J.D.; Methodology, J.D.; Data curation, J.D.; Writing—original draft, J.D.; Methodology, Z.X.; Data curation, Z.X.; Formal analysis, Z.X.; Data curation, Z.Y.; Writing—review and editing, Z.Y.; Supervision, Z.Y.; Writing—review and editing, J.J.; Funding acquisition, J.J.; Supervision, J.J. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the National Natural Science Foundation of China (21677012) to J.J.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The experimental data used to support the findings of this study are included in the article. And more detailed data are available from the corresponding author upon request.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Aeschbacher, M.; Sander, M.; Schwarzenbach, R.P. Novel Electrochemical Approach to Assess the Redox Properties of Humic Substances. Environ. Sci. Technol. 2010, 44, 87–93. [Google Scholar] [CrossRef] [PubMed]
  2. Bauer, M.; Heitmann, T.; Macalady, D.L.; Blodau, C. Electron Transfer Capacities and Reaction Kinetics of Peat Dissolved Organic Matter. Environ. Sci. Technol. 2007, 41, 139–145. [Google Scholar] [CrossRef] [PubMed]
  3. Bolan, N.S.; Adriano, D.C.; Kunhikrishnan, A.; James, T.; McDowell, R.; Senesi, N. Dissolved organic matter: Biogeochemistry, dynamics, and environmental significance in soils. In Advances in Agronomy; Elsevier: Amsterdam, The Netherlands, 2011; Volume 110, pp. 1–75. [Google Scholar]
  4. Lv, J.; Han, R.; Huang, Z.; Luo, L.; Cao, D.; Zhang, S. Relationship between Molecular Components and Reducing Capacities of Humic Substances. ACS Earth Space Chem. 2018, 2, 330–339. [Google Scholar] [CrossRef]
  5. Zou, J.; Huang, J.; Yue, D.; Zhang, H. Roles of oxygen and Mn (IV) oxide in abiotic formation of humic substances by oxidative polymerization of polyphenol and amino acid. Chem. Eng. J. 2020, 393, 124734. [Google Scholar] [CrossRef]
  6. Jiang, T.; Skyllberg, U.; Wei, S.; Wang, D.; Lu, S.; Jiang, Z.; Flanagan, D.C. Modeling of the structure-specific kinetics of abiotic, dark reduction of Hg(II) complexed by O/N and S functional groups in humic acids while accounting for time-dependent structural rearrangement. Geochim. Cosmochim. Acta 2015, 154, 151–167. [Google Scholar] [CrossRef]
  7. Piccolo, A. The supramolecular structure of humic substances. Soil. Sci. 2001, 166, 810–832. [Google Scholar] [CrossRef] [Green Version]
  8. Simpson, A.J.; Kingery, W.L.; Hayes, M.H.B.; Spraul, M.; Humpfer, E.; Dvortsak, P.; Kerssebaum, R.; Godejohann, M.; Hofmann, M. Molecular structures and associations of humic substances in the terrestrial environment. Naturwissenschaften 2002, 89, 84–88. [Google Scholar] [CrossRef]
  9. Sutton, R.; Sposito, G. Molecular Structure in Soil Humic Substances: The New View. Environ. Sci. Technol. 2005, 39, 9009–9015. [Google Scholar] [CrossRef]
  10. Yang, Z.; Kappler, A.; Jiang, J. Reducing Capacities and Distribution of Redox-Active Functional Groups in Low Molecular Weight Fractions of Humic Acids. Environ. Sci. Technol. 2016, 50, 12105–12113. [Google Scholar] [CrossRef] [PubMed]
  11. Tan, W.; Xi, B.; Wang, G.; Jiang, J.; He, X.; Mao, X.; Gao, R.; Huang, C.; Zhang, H.; Li, D.; et al. Increased Electron-Accepting and Decreased Electron-Donating Capacities of Soil Humic Substances in Response to Increasing Temperature. Environ. Sci. Technol. 2017, 51, 3176–3186. [Google Scholar] [CrossRef] [PubMed]
  12. Xu, Z.; Yang, Z.; Wang, H.; Jiang, J. Assessing Redox Properties of Natural Organic Matters with regard to Electron Exchange Capacity and Redox-Active Functional Groups. J. Chem. 2020, 2020, 2698213. [Google Scholar] [CrossRef]
  13. Dryer, D.J.; Korshin, G.V.; Fabbricino, M. In Situ Examination of the Protonation Behavior of Fulvic Acids Using Differential Absorbance Spectroscopy. Environ. Sci. Technol. 2008, 42, 6644–6649. [Google Scholar] [CrossRef]
  14. Phillips, S.M.; Bellcross, A.D.; Smith, G.D. Light Absorption by Brown Carbon in the Southeastern United States is pH-dependent. Environ. Sci. Technol. 2017, 51, 6782–6790. [Google Scholar] [CrossRef]
  15. Boyle, E.S.; Guerriero, N.; Thiallet, A.; Del Vecchio, R.; Blough, N.V. Optical Properties of Humic Substances and CDOM: Relation to Structure. Environ. Sci. Technol. 2009, 43, 2262–2268. [Google Scholar] [CrossRef] [PubMed]
  16. Del Vecchio, R.; Blough, N.V. On the Origin of the Optical Properties of Humic Substances. Environ. Sci. Technol. 2004, 38, 3885–3891. [Google Scholar] [CrossRef] [PubMed]
  17. Sharpless, C.; Blough, N.V. The importance of charge-transfer interactions in determining chromophoric dissolved organic matter (CDOM) optical and photochemical properties. Environ. Sci. Process. Impacts 2014, 16, 654–671. [Google Scholar] [CrossRef]
  18. Cao, J.; Jiang, J. Reducing capacities in continuously released low molecular weight fractions from bulk humic acids. J. Environ. Manag. 2019, 244, 172–179. [Google Scholar] [CrossRef] [PubMed]
  19. Straub, K.L.; Benz, M.; Schink, B. Iron metabolism in anoxic environments at near neutral pH. FEMS Microbiol. Ecol. 2001, 34, 181–186. [Google Scholar] [CrossRef]
  20. Szilágyi, M. Reduction of Fe3+ ion by humic acid preparations. Soil Sci. 1971, 111, 233–235. [Google Scholar] [CrossRef]
  21. Struyk, Z.; Sposito, G. Redox properties of standard humic acids. Geoderma 2001, 102, 329–346. [Google Scholar] [CrossRef]
  22. Borch, T.; Kretzschmar, R.; Kappler, A.; Van Cappellen, P.; Ginder-Vogel, M.; Voegelin, A.; Campbell, K. Biogeochemical Redox Processes and their Impact on Contaminant Dynamics. Environ. Sci. Technol. 2010, 44, 15–23. [Google Scholar] [CrossRef]
  23. Klausen, J.; Troeber, S.P.; Haderlein, S.B.; Schwarzenbach, R.P. Reduction of Substituted Nitrobenzenes by Fe(II) in Aqueous Mineral Suspensions. Environ. Sci. Technol. 1995, 29, 2396–2404. [Google Scholar] [CrossRef]
  24. Charlet, L.; Scheinost, A.; Tournassat, C.; Greneche, J.; Géhin, A.; Fernández-Martínez, A.; Coudert, S.; Tisserand, D.; Brendle, J. Electron transfer at the mineral/water interface: Selenium reduction by ferrous iron sorbed on clay. Geochim. Cosmochim. Acta 2007, 71, 5731–5749. [Google Scholar] [CrossRef] [Green Version]
  25. Liu, D.; Zhang, Q.; Wu, L.; Zeng, Q.; Dong, H.; Bishop, M.E.; Wang, H. Humic acid-enhanced illite and talc formation associated with microbial reduction of Fe(III) in nontronite. Chem. Geol. 2016, 447, 199–207. [Google Scholar] [CrossRef]
  26. Konhauser, K.O.; Kappler, A.; Roden, E.E. Iron in microbial metabolisms. Elements 2011, 7, 89–93. [Google Scholar] [CrossRef]
  27. Melton, E.D.; Swanner, E.D.; Behrens, S.; Schmidt, C.; Kappler, A. The interplay of microbially mediated and abiotic reactions in the biogeochemical Fe cycle. Nat. Rev. Genet. 2014, 12, 797–808. [Google Scholar] [CrossRef]
  28. Okamoto, A.; Nakamura, R.; Nealson, K.H.; Hashimoto, K. Bound Flavin Model Suggests Similar Electron-Transfer Mechanisms in Shewanella and Geobacter. ChemElectroChem 2014, 1, 1808–1812. [Google Scholar] [CrossRef]
  29. Benner, S.G.; Hansel, C.M.; Wielinga, B.W.; Barber, T.M.; Fendorf, S. Reductive Dissolution and Biomineralization of Iron Hydroxide under Dynamic Flow Conditions. Environ. Sci. Technol. 2002, 36, 1705–1711. [Google Scholar] [CrossRef] [PubMed]
  30. Cummings, D.E.; Caccavo, F.; Fendorf, S.; Rosenzweig, R.F. Arsenic Mobilization by the Dissimilatory Fe(III)-Reducing Bacterium Shewanella alga BrY. Environ. Sci. Technol. 1999, 33, 723–729. [Google Scholar] [CrossRef]
  31. Lovley, D.R.; Coates, J.D.; Blunt-Harris, E.L.; Phillips, E.J.P.; Woodward, J.C. Humic substances as electron acceptors for microbial respiration. Nature 1996, 382, 445–448. [Google Scholar] [CrossRef]
  32. Sposito, G. Electron Shuttling by Natural Organic Matter: Twenty Years After. ACS Symp. Ser. 2011, 1071, 113–127. [Google Scholar] [CrossRef]
  33. Rakshit, S.; Sarkar, D. Assessing redox properties of standard humic substances. Int. J. Environ. Sci. Technol. 2017, 14, 1497–1504. [Google Scholar] [CrossRef]
  34. Han, R.; Liu, T.; Li, F.; Li, X.; Chen, D.; Wu, Y. Dependence of Secondary Mineral Formation on Fe(II) Production from Ferrihydrite Reduction by Shewanella oneidensis MR-1. ACS Earth Space Chem. 2018, 2, 399–409. [Google Scholar] [CrossRef]
  35. Kumar, A.; Hsu, L.H.H.; Kavanagh, P.; Barrière, F.; Lens, P.N.; Lapinsonnière, L.; Schröder, U.; Jiang, X.; Leech, D. The ins and outs of microorganism–electrode electron transfer reactions. Nat. Rev. Chem. 2017, 1, 24. [Google Scholar] [CrossRef]
  36. Pirbadian, S.; Chavez, M.S.; El-Naggar, M.Y. Spatiotemporal mapping of bacterial membrane potential responses to extracellular electron transfer. Proc. Natl. Acad. Sci. USA 2020, 117, 20171–20179. [Google Scholar] [CrossRef] [PubMed]
  37. Xu, S.; Jangir, Y.; El-Naggar, M.Y. Disentangling the roles of free and cytochrome-bound flavins in extracellular electron transport from Shewanella oneidensis MR-1. Electrochim. Acta 2016, 198, 49–55. [Google Scholar] [CrossRef] [Green Version]
  38. Cornell, R.M.; Schwertmann, U. The Iron Oxide; Wiley-VCH: New York, NY, USA, 2003; ISBN 3-527-30274-3. [Google Scholar]
  39. Stookey, L. Ferrozine—A new spectrophotometric reagent for iron. Anal. Chem. 1970, 42, 779–781. [Google Scholar] [CrossRef] [Green Version]
  40. Peuravuori, J.; Pihlaja, K. Molecular size distribution and spectroscopic properties of aquatic humic substances. Anal. Chim. Acta 1997, 337, 133–149. [Google Scholar] [CrossRef]
  41. Fox, L. The removal of dissolved humic acid during estuarine mixing. Estuar. Coast. Shelf Sci. 1983, 16, 431–440. [Google Scholar] [CrossRef]
  42. Fooken, U.; Liebezeit, G. Distinction of marine and terrestrial origin of humic acids in North Sea surface sediments by absorption spectroscopy. Mar. Geol. 2000, 164, 173–181. [Google Scholar] [CrossRef]
  43. Mao, J.-D.; Tremblay, L.; Gagné, J.-P.; Kohl, S.; Rice, J.; Schmidt-Rohr, K. Humic acids from particulate organic matter in the Saguenay Fjord and the St. Lawrence Estuary investigated by advanced solid-state NMR. Geochim. Cosmochim. Acta 2007, 71, 5483–5499. [Google Scholar] [CrossRef]
  44. Mahoney, D.T.; Al Aamery, N.; Fox, J.F.; Riddle, B.; Ford, W.; Wang, Y.T. Equilibrium sediment exchange in the earth’s critical zone: Evidence from sediment fingerprinting with stable isotopes and watershed modeling. J. Soils Sediments 2019, 19, 3332–3356. [Google Scholar] [CrossRef]
  45. Kim, J.; Cho, H.-M.; Kim, G. Significant production of humic fluorescent dissolved organic matter in the continental shelf waters of the northwestern Pacific Ocean. Sci. Rep. 2018, 8, 4887. [Google Scholar] [CrossRef] [PubMed]
  46. Bravo, C.; Millo, C.; Covelli, S.; Contin, M.; De Nobili, M. Terrestrial-marine continuum of sedimentary natural organic matter in a mid-latitude estuarine system. J. Soils Sediments 2019, 20, 1074–1086. [Google Scholar] [CrossRef]
  47. Goñi, M.A.; Teixeira, M.J.; Perkey, D.W. Sources and distribution of organic matter in a river-dominated estuary (Winyah Bay, SC, USA). Estuar. Coast. Shelf Sci. 2003, 57, 1023–1048. [Google Scholar] [CrossRef]
  48. Otero, E.; Culp, R.; E Noakes, J.; E Hodson, R. The distribution and δ13C of dissolved organic carbon and its humic fraction in estuaries of southeastern USA. Estuar. Coast. Shelf Sci. 2003, 56, 1187–1194. [Google Scholar] [CrossRef]
  49. Aeschbacher, M.; Graf, C.; Schwarzenbach, R.P.; Sander, M. Antioxidant Properties of Humic Substances. Environ. Sci. Technol. 2012, 46, 4916–4925. [Google Scholar] [CrossRef]
  50. Roden, E.E.; Kappler, A.; Bauer, I.; Jiang, J.; Paul, A.; Stoesser, R.; Konishi, H.; Xu, H. Extracellular electron transfer through microbial reduction of solid-phase humic substances. Nat. Geosci. 2010, 3, 417–421. [Google Scholar] [CrossRef]
  51. Lovley, D.R.; Fraga, J.L.; Blunt-Harris, E.L.; Hayes, L.A.; Phillips, E.J.P.; Coates, J.D. Humic Substances as a Mediator for Microbially Catalyzed Metal Reduction. Acta Hydrochim. Hydrobiol. 1998, 26, 152–157. [Google Scholar] [CrossRef]
  52. Klüpfel, L.; Piepenbrock, A.; Kappler, A.; Sander, M. Humic substances as fully regenerable electron acceptors in recurrently anoxic environments. Nat. Geosci. 2014, 7, 195–200. [Google Scholar] [CrossRef]
  53. Ratasuk, N.; Nanny, M.A. Characterization and Quantification of Reversible Redox Sites in Humic Substances. Environ. Sci. Technol. 2007, 41, 7844–7850. [Google Scholar] [CrossRef] [PubMed]
Ijerph 18 06807 g001 550
Figure 1. The I–t curve of different molecular weight fractions of HA in direct electrochemical oxidation experiments (The embedded picture is the I–t curve within 3 min of reaction.) (A) LHA; (B) PPHA.
Figure 1. The I–t curve of different molecular weight fractions of HA in direct electrochemical oxidation experiments (The embedded picture is the I–t curve within 3 min of reaction.) (A) LHA; (B) PPHA.
Ijerph 18 06807 g001
Ijerph 18 06807 g002 550
Figure 2. The EDC of different molecular weight fractions of LHA under +0.61 V direct electrochemical oxidation experiments. (A) LHA; (B) PPHA.
Figure 2. The EDC of different molecular weight fractions of LHA under +0.61 V direct electrochemical oxidation experiments. (A) LHA; (B) PPHA.
Ijerph 18 06807 g002
Ijerph 18 06807 g003 550
Figure 3. The I–t curve of different molecular weight fractions of LHA and PPHA in direct electrochemical reduction, which was carried out at Eh = −0.49 V, Eh = −0.59 V, and Eh = −0.69 V for 3 h: (A) LHA −0.49 V; (B) LHA −0.59 V; (C) LHA −0.69 V; (D) PPHA −0.49 V; (E) PPHA −0.59 V; (F) PPHA −0.69 V.
Figure 3. The I–t curve of different molecular weight fractions of LHA and PPHA in direct electrochemical reduction, which was carried out at Eh = −0.49 V, Eh = −0.59 V, and Eh = −0.69 V for 3 h: (A) LHA −0.49 V; (B) LHA −0.59 V; (C) LHA −0.69 V; (D) PPHA −0.49 V; (E) PPHA −0.59 V; (F) PPHA −0.69 V.
Ijerph 18 06807 g003
Ijerph 18 06807 g004a 550Ijerph 18 06807 g004b 550
Figure 4. The EAC of different molecular weight fractions of HA under Eh = −0.49 V, Eh = −0.59 V, and Eh = −0.69 V direct electrochemical reduction experiments. (A) LHA; (B) PPHA.
Figure 4. The EAC of different molecular weight fractions of HA under Eh = −0.49 V, Eh = −0.59 V, and Eh = −0.69 V direct electrochemical reduction experiments. (A) LHA; (B) PPHA.
Ijerph 18 06807 g004aIjerph 18 06807 g004b
Ijerph 18 06807 g005 550
Figure 5. Amount of Fe (II) formation in the microbial (Shewanella oneidensis MR-1) Fh reduction process in the presence and absence of different molecular weight fractions of LHA and PPHA.
Figure 5. Amount of Fe (II) formation in the microbial (Shewanella oneidensis MR-1) Fh reduction process in the presence and absence of different molecular weight fractions of LHA and PPHA.
Ijerph 18 06807 g005
Ijerph 18 06807 g006 550
Figure 6. Comparison of electron shuttle capability between LHA and PPHA with different molecular weight.
Figure 6. Comparison of electron shuttle capability between LHA and PPHA with different molecular weight.
Ijerph 18 06807 g006
Ijerph 18 06807 g007 550
Figure 7. Comparison in per gram carbon ETC between electrochemical reduction and microbial reduction of HA with different molecular weight fractions. (A) LHA (B) PPHA.
Figure 7. Comparison in per gram carbon ETC between electrochemical reduction and microbial reduction of HA with different molecular weight fractions. (A) LHA (B) PPHA.
Ijerph 18 06807 g007
Table
Table 1. TOC contents of different molecular weight fractions of LHA and PPHA after 72 h dialysis.
Table 1. TOC contents of different molecular weight fractions of LHA and PPHA after 72 h dialysis.
TOC (mg C/L)3500-LMWF14,000-LMWF3500-Retentate14,000-RetentateBulk3500-LMWF/Bulk14,000-LMWF/Bulk
PPHA8.4811.62210.90198.70234.903.61%4.95%
LHA4.619.14217.18195.74228.002.02%4.01%
Table
Table 2. Comparison in ETC between electrochemical reduction and microbial reduction of HA with different molecular weight fractions.
Table 2. Comparison in ETC between electrochemical reduction and microbial reduction of HA with different molecular weight fractions.
ETC (μmol e-)Electrochemical ReducedMicrobial Reduced
−0.49 V−0.59 V−0.69 V
PPHA3500-LMWF0.140.621.200.60
14,000-LMWF0.110.621.120.68
3500 retentate0.150.591.430.82
14,000 retentate0.351.532.140.78
bulk0.431.572.330.92
LHA3500-LMWF0.030.401.040.56
14,000-LMWF0.030.541.030.58
3500 retentate0.040.791.760.62
14,000 retentate0.050.962.170.62
bulk0.061.142.160.78
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Duan, J.; Xu, Z.; Yang, Z.; Jiang, J. Insight to Microbial Fe(III) Reduction Mediated by Redox-Active Humic Acids with Varied Redox Potentials. Int. J. Environ. Res. Public Health 2021, 18, 6807. https://doi.org/10.3390/ijerph18136807

AMA Style

Duan J, Xu Z, Yang Z, Jiang J. Insight to Microbial Fe(III) Reduction Mediated by Redox-Active Humic Acids with Varied Redox Potentials. International Journal of Environmental Research and Public Health. 2021; 18(13):6807. https://doi.org/10.3390/ijerph18136807

Chicago/Turabian Style

Duan, Jingtao, Zhiyuan Xu, Zhen Yang, and Jie Jiang. 2021. "Insight to Microbial Fe(III) Reduction Mediated by Redox-Active Humic Acids with Varied Redox Potentials" International Journal of Environmental Research and Public Health 18, no. 13: 6807. https://doi.org/10.3390/ijerph18136807

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop