Role of clay-associated humic substances in catalyzing bioreduction of structural Fe(III) in nontronite by Shewanella putrefaciens CN32

Hongyan Zuo; Ravi Kukkadapu; Zihua Zhu; Shuisong Ni; Liuqin Huang; Qiang Zeng; Chongxuan Liu; Hailiang Dong

doi:10.1016/j.scitotenv.2020.140213

Role of clay-associated humic substances in catalyzing bioreduction of structural Fe(III) in nontronite by Shewanella putrefaciens CN32

Sci Total Environ. 2020 Nov 1:741:140213. doi: 10.1016/j.scitotenv.2020.140213. Epub 2020 Jun 19.

Authors

Hongyan Zuo¹, Ravi Kukkadapu², Zihua Zhu², Shuisong Ni³, Liuqin Huang⁴, Qiang Zeng⁵, Chongxuan Liu⁶, Hailiang Dong⁷

Affiliations

¹ Department of Geology and Environmental Earth Science, Miami University, Oxford, OH 45056, USA.
² Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, P.O. Box 999, Richland, Washington 99354, USA.
³ Department of Chemistry and Biochemistry, Miami University, Oxford, OH 45056, USA.
⁴ State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan 430074, China.
⁵ State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Beijing 100083, China.
⁶ School of Environmental Science and Engineering, Southern University of Science and Technology, Shenzhen 518055, China.
⁷ Department of Geology and Environmental Earth Science, Miami University, Oxford, OH 45056, USA; State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Beijing 100083, China. Electronic address: dongh@miamioh.edu.

PMID: 32603937
DOI: 10.1016/j.scitotenv.2020.140213

Abstract

Previous studies have shown that humic substances can serve as electron shuttle to catalyze bioreduction of structural Fe(III) in clay minerals, but it is unclear if clay-sorbed humic substances can serve the same function. It is unknown if the electron shuttling function is dependent on electron donor type and if humic substances undergo change as a result. In this study, humic acid (HA) and fulvic acid (FA) were sorbed onto nontronite (NAu-2) surface. Structural Fe(III) in HA- and FA-coated NAu-2 samples was bioreduced by Shewanella putrefaciens CN32 using H₂ and lactate as electron donors. The results showed a contrasting effect of humic substances on bioreduction of structural Fe(III), depending on the electron donor type. With H₂ as electron donor, humic substances had little effect on bioreduction of Fe(III) (the reduction extent: 26.2%, 27.4%, 29.3% for HA-coated, FA-coated, and uncoated NAu-2, respectively). In contrast, these substances significantly enhanced bioreduction of Fe(III) with lactate as electron donor (the reduction extent: 20.2%, 20.7%, 11.5% for HA-coated, FA-coated, and uncoated NAu-2, respectively). This contrasting behavior is likely caused by the difference in reaction free energy and electron transport process between H₂ and lactate. When H₂ served as electron donor, more energy was released than when lactate served as electron donor. In addition, because of different cellular locations of lactate dehydrogenase (inner membrane) and H₂ hydrogenase (the periplasm), electrons generated by H₂ hydrogenase may pass through the electron transport chain more rapidly than those generated from lactate dehydrogenase. Through their functions as electron shuttle and/or carbon source, clay-sorbed HA/FA underwent partial transformation to amino acids and other compounds. The availability of external carbon source played an important role in the amount and type of secondary product generation. These results have important implications for coupled iron and carbon biogeochemical cycles in clay- and humic substance-rich environments.

Keywords: H2; Humic substances; Iron reduction; Lactate; Nontronite; Shewanella putrefaciens CN32.

MeSH terms

Clay
Ferric Compounds
Humic Substances
Iron
Oxidation-Reduction
Shewanella putrefaciens*

Substances

Ferric Compounds
Humic Substances
Iron
Clay