Humic substances as electron acceptor for anaerobic oxidation of methane (AOM) and electron shuttle in Mn (IV)-dependent AOM

Mengying Xie; Xueqin Zhang; Shiqing Li; Nova Maulani; Fangrui Cai; Yue Zheng; Chen Cai; Bernardino Virdis; Zhiguo Yuan; Shihu Hu

doi:10.1016/j.scitotenv.2023.169576

Humic substances as electron acceptor for anaerobic oxidation of methane (AOM) and electron shuttle in Mn (IV)-dependent AOM

Mengying Xie
, Xueqin Zhang^*
, Shiqing Li
, Nova Maulani
, Fangrui Cai
, Yue Zheng
, Chen Cai
, Bernardino Virdis
, Zhiguo Yuan
, Shihu Hu

^*Corresponding author for this work

School of Energy and Environment

Research output: Journal Publications and Reviews › RGC 21 - Publication in refereed journal › peer-review

27 Citations (Scopus)

139 Downloads (CityUHK Scholars)

Abstract

Anaerobic methanotrophic archaea (ANME) belonging to the family Methanoperedenaceae are crucial for the global carbon cycle and different biogeochemical processes, owing to their metabolic versatility to couple anaerobic oxidation of methane (AOM) with different electron acceptors. A universal feature of Methanoperedenaceae is the abundant genes encoded in their genomes associated with extracellular electron transfer (EET) pathways. Candidatus. ‘Methanoperedens manganicus’, an archaeon belonging to the family Methanoperedenaceae, was recently enriched in a bioreactor performing AOM coupled with Mn (IV) reduction. Using this EET-capable ANME, we tested the hypothesis in this study that ANME can catalyse the humic-dependent AOM for growth. A two-year incubation showed that AOM activity can be sustained by Ca. ‘M. manganicus’ consortium in a bioreactor fed only with humic acids and methane. An isotopic mass balance batch test confirmed that the observed AOM was coupled to the reduction of humic acids. The increase of relative abundance of Ca. ‘M. manganicus’, and the total archaea population in the microbial community suggested that Ca. ‘M. manganicus’ can grow on methane and humic acids. The observation of humic-dependent AOM led to a subsequent hypothesis that humic acids could be used as the electron shuttle to mediate the EET in dissimilatory Mn (IV) reduction by Ca. ‘M. manganicus’. We tested this hypothesis by adding humic acids to a Ca. ‘M. manganicus’ dominated-culture, which showed that the AOM rate was doubled by the addition of humic acids. X-ray photoelectron spectroscopy (XPS) showed that quinone moieties were consumed when humic acids worked as electron acceptors while remaining stable when functioning as a shuttle for electron transfer. The results of our study suggest that humic acids may serve as electron shuttles to allow ANME to access more electron acceptors through long-range EET. © 2023 The Authors

Original language	English
Article number	169576
Number of pages	11
Journal	Science of the Total Environment
Volume	912
Online published	23 Dec 2023
DOIs	https://doi.org/10.1016/j.scitotenv.2023.169576
Publication status	Published - 20 Feb 2024

Funding

This work was supported by the Australian Research Council (ARC) through the projects of the Australian Laureate Fellowship (FL170100086). M.X. is supported by the UQ Research Training Scholarship. Y.Z. acknowledges support from National Natural Science Foundation of China (42276117). C.C. acknowledges the support from the National Natural Science Foundation of China (NSFC 42277106), the USTC Research Funds of the Double First-Class Initiative (YD2400002006) and the Fundamental Research Funds for the Central Universities (WK3530000016).

Research Keywords

Anaerobic oxidation of methane (AOM)
electron shuttle
Extracellular electron transfer (EET)
Humicdependent AOM
Methanoperedenaceae

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@article{8ebc313a49fc4e2ba3baeb39fb144a3b,

title = "Humic substances as electron acceptor for anaerobic oxidation of methane (AOM) and electron shuttle in Mn (IV)-dependent AOM",

abstract = "Anaerobic methanotrophic archaea (ANME) belonging to the family Methanoperedenaceae are crucial for the global carbon cycle and different biogeochemical processes, owing to their metabolic versatility to couple anaerobic oxidation of methane (AOM) with different electron acceptors. A universal feature of Methanoperedenaceae is the abundant genes encoded in their genomes associated with extracellular electron transfer (EET) pathways. Candidatus. {\textquoteleft}Methanoperedens manganicus{\textquoteright}, an archaeon belonging to the family Methanoperedenaceae, was recently enriched in a bioreactor performing AOM coupled with Mn (IV) reduction. Using this EET-capable ANME, we tested the hypothesis in this study that ANME can catalyse the humic-dependent AOM for growth. A two-year incubation showed that AOM activity can be sustained by Ca. {\textquoteleft}M. manganicus{\textquoteright} consortium in a bioreactor fed only with humic acids and methane. An isotopic mass balance batch test confirmed that the observed AOM was coupled to the reduction of humic acids. The increase of relative abundance of Ca. {\textquoteleft}M. manganicus{\textquoteright}, and the total archaea population in the microbial community suggested that Ca. {\textquoteleft}M. manganicus{\textquoteright} can grow on methane and humic acids. The observation of humic-dependent AOM led to a subsequent hypothesis that humic acids could be used as the electron shuttle to mediate the EET in dissimilatory Mn (IV) reduction by Ca. {\textquoteleft}M. manganicus{\textquoteright}. We tested this hypothesis by adding humic acids to a Ca. {\textquoteleft}M. manganicus{\textquoteright} dominated-culture, which showed that the AOM rate was doubled by the addition of humic acids. X-ray photoelectron spectroscopy (XPS) showed that quinone moieties were consumed when humic acids worked as electron acceptors while remaining stable when functioning as a shuttle for electron transfer. The results of our study suggest that humic acids may serve as electron shuttles to allow ANME to access more electron acceptors through long-range EET. {\textcopyright} 2023 The Authors",

keywords = "Anaerobic oxidation of methane (AOM), electron shuttle, Extracellular electron transfer (EET), Humicdependent AOM, Methanoperedenaceae",

author = "Mengying Xie and Xueqin Zhang and Shiqing Li and Nova Maulani and Fangrui Cai and Yue Zheng and Chen Cai and Bernardino Virdis and Zhiguo Yuan and Shihu Hu",

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doi = "10.1016/j.scitotenv.2023.169576",

language = "English",

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journal = "Science of the Total Environment",

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T1 - Humic substances as electron acceptor for anaerobic oxidation of methane (AOM) and electron shuttle in Mn (IV)-dependent AOM

AU - Xie, Mengying

AU - Zhang, Xueqin

AU - Li, Shiqing

AU - Maulani, Nova

AU - Cai, Fangrui

AU - Zheng, Yue

AU - Cai, Chen

AU - Virdis, Bernardino

AU - Yuan, Zhiguo

AU - Hu, Shihu

PY - 2024/2/20

Y1 - 2024/2/20

N2 - Anaerobic methanotrophic archaea (ANME) belonging to the family Methanoperedenaceae are crucial for the global carbon cycle and different biogeochemical processes, owing to their metabolic versatility to couple anaerobic oxidation of methane (AOM) with different electron acceptors. A universal feature of Methanoperedenaceae is the abundant genes encoded in their genomes associated with extracellular electron transfer (EET) pathways. Candidatus. ‘Methanoperedens manganicus’, an archaeon belonging to the family Methanoperedenaceae, was recently enriched in a bioreactor performing AOM coupled with Mn (IV) reduction. Using this EET-capable ANME, we tested the hypothesis in this study that ANME can catalyse the humic-dependent AOM for growth. A two-year incubation showed that AOM activity can be sustained by Ca. ‘M. manganicus’ consortium in a bioreactor fed only with humic acids and methane. An isotopic mass balance batch test confirmed that the observed AOM was coupled to the reduction of humic acids. The increase of relative abundance of Ca. ‘M. manganicus’, and the total archaea population in the microbial community suggested that Ca. ‘M. manganicus’ can grow on methane and humic acids. The observation of humic-dependent AOM led to a subsequent hypothesis that humic acids could be used as the electron shuttle to mediate the EET in dissimilatory Mn (IV) reduction by Ca. ‘M. manganicus’. We tested this hypothesis by adding humic acids to a Ca. ‘M. manganicus’ dominated-culture, which showed that the AOM rate was doubled by the addition of humic acids. X-ray photoelectron spectroscopy (XPS) showed that quinone moieties were consumed when humic acids worked as electron acceptors while remaining stable when functioning as a shuttle for electron transfer. The results of our study suggest that humic acids may serve as electron shuttles to allow ANME to access more electron acceptors through long-range EET. © 2023 The Authors

AB - Anaerobic methanotrophic archaea (ANME) belonging to the family Methanoperedenaceae are crucial for the global carbon cycle and different biogeochemical processes, owing to their metabolic versatility to couple anaerobic oxidation of methane (AOM) with different electron acceptors. A universal feature of Methanoperedenaceae is the abundant genes encoded in their genomes associated with extracellular electron transfer (EET) pathways. Candidatus. ‘Methanoperedens manganicus’, an archaeon belonging to the family Methanoperedenaceae, was recently enriched in a bioreactor performing AOM coupled with Mn (IV) reduction. Using this EET-capable ANME, we tested the hypothesis in this study that ANME can catalyse the humic-dependent AOM for growth. A two-year incubation showed that AOM activity can be sustained by Ca. ‘M. manganicus’ consortium in a bioreactor fed only with humic acids and methane. An isotopic mass balance batch test confirmed that the observed AOM was coupled to the reduction of humic acids. The increase of relative abundance of Ca. ‘M. manganicus’, and the total archaea population in the microbial community suggested that Ca. ‘M. manganicus’ can grow on methane and humic acids. The observation of humic-dependent AOM led to a subsequent hypothesis that humic acids could be used as the electron shuttle to mediate the EET in dissimilatory Mn (IV) reduction by Ca. ‘M. manganicus’. We tested this hypothesis by adding humic acids to a Ca. ‘M. manganicus’ dominated-culture, which showed that the AOM rate was doubled by the addition of humic acids. X-ray photoelectron spectroscopy (XPS) showed that quinone moieties were consumed when humic acids worked as electron acceptors while remaining stable when functioning as a shuttle for electron transfer. The results of our study suggest that humic acids may serve as electron shuttles to allow ANME to access more electron acceptors through long-range EET. © 2023 The Authors

KW - Anaerobic oxidation of methane (AOM)

KW - electron shuttle

KW - Extracellular electron transfer (EET)

KW - Humicdependent AOM

KW - Methanoperedenaceae

UR - https://www.scopus.com/pages/publications/85181721672

UR - https://www.scopus.com/pages/publications/85181721672#tab=impact

U2 - 10.1016/j.scitotenv.2023.169576

DO - 10.1016/j.scitotenv.2023.169576

M3 - RGC 21 - Publication in refereed journal

C2 - 38145665

SN - 0048-9697

VL - 912

JO - Science of the Total Environment

JF - Science of the Total Environment

M1 - 169576

ER -

Humic substances as electron acceptor for anaerobic oxidation of methane (AOM) and electron shuttle in Mn (IV)-dependent AOM

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