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Objective The survival mechanisms of aerobic methylotrophs in oxygen-deficient environments represent a focal topic in current microbial ecology. This study aims to investigate the extracellular electron transfer (EET) mechanism by which the aerobic methylotroph Methylophilus sp. 14 utilizes insoluble iron minerals (ferrihydrite) under oxygen-deficient conditions and to elucidate the synergistic role of exogenous and endogenous electron shuttles in this process. Methods Anaerobic culture (initial O2 level: 2%) of Methylophilus sp. 14 isolated from sediments of Fuxian Lake was conducted with methanol as the carbon source and ferrihydrite as the sole terminal electron acceptor. Iron reduction kinetics were measured along with electrochemical analyses (differential pulse voltammetry and cyclic voltammetry) and microscopic characterization (scanning/transmission electron microscopy) to systematically evaluate the iron-reducing capacity of the strain and explore the roles of exogenous shuttles (humic substances, HS; anthraquinone-2,6-disulfonate, AQDS) and endogenous flavins in electron transfer. Results Methylophilus sp. 14 coupled methanol oxidation with ferrihydrite reduction, increasing the Fe(II) concentration from 0.49 μmol/L to 8.29 μmol/L within 20 days and promoting the partial transformation of ferrihydrite into magnetite. Exogenous addition of HS and AQDS further enhanced Fe(II) production to 10.73 μmol/L and 11.22 μmol/L, respectively, improving the cumulative electron transfer efficiency by approximately 1.5 folds. Electrochemical analyses indicated that the redox potential of the bacterial cells was lower than that of ferrihydrite, thermodynamically favoring spontaneous electron transfer. Soluble AQDS formed a conductive microenvironment that accelerated electron flux. Notably, this study first revealed that Methylophilus sp. 14 synthesized and secreted flavins, whose extracellular concentration showed a strong positive correlation with the EET rate (r=0.94, P<0.001). Furthermore, exogenous shuttles stimulated increases of 30%‒50% in total flavin secretion. Flavins functioned as a critical electron bridge, mediating electron transfer from intracellular metabolism to exogenous shuttles and thereby establishing a cooperative electron transport chain. Conclusion This work reveals a novel EET strategy employed by aerobic methylotrophs to adapt to oxygen-deficient conditions. That is, exogenous electron shuttles not only construct an extracellular conductive microenvironment but also stimulate the secretion of endogenous flavins, resulting in a synergistic electron transfer mechanism that efficiently drives the reduction of solid-phase iron minerals. These findings deepen our understanding of the metabolic flexibility of aerobic microorganisms and their ecological role at aerobic-anerobic interfaces.
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| 科 Family | 属数 Number of genus | 种数 Number of species | 占总种数比例 Percentage of total species (%) | 属 Genus | 种数 Number of species | 占总种数比例 Percentage of total species (%) |
|---|---|---|---|---|---|---|
| 鹅膏菌科Amanitaceae | 2 | 11 | 5.26 | 鹅膏菌属 Amanita | 10 | 4.78 |
| 小菇科 Mycenaceae | 2 | 12 | 5.74 | 丝盖伞属 Inocybe | 5 | 2.39 |
| 多孔菌科 Polyporaceae | 8 | 14 | 6.70 | 蜡蘑属 Laccaria | 5 | 2.39 |
| 红菇科 Russulaceae | 3 | 23 | 11.00 | 小皮伞属 Marasmius | 6 | 2.87 |
| 小菇属 Mycena | 11 | 5.26 | ||||
| 光柄菇属 Pluteus | 5 | 2.39 | ||||
| 红菇属 Russula | 17 | 8.13 | ||||
| 栓菌属 Trametes | 5 | 2.39 |
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