1. CAS Key Laboratory of Urban Pollutant Conversion, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China 2. University of Chinese Academy of Sciences, Beijing 100049, China
● Term of manganese-oxidizing microorganisms should be reconsidered.
● Visible light induces heterotrophic bacteria to produce superoxide.
● Heterotrophic bacteria oxidize Mn(II) ions with a fast oxidation rate.
● Superoxide oxidizing Mn(II) ions is an unintended side reaction of bacteria.
● Superoxide is an important oxidation force of Mn(II) in the environment.
Manganese oxides are widely distributed in soils and sediments, affecting the migration and transformation of heavy metals and organic pollutants. The microbial conversion of soluble Mn(II) into insoluble Mn(III/IV) oxides is considered to be the initial source of manganese oxides in the environment; however, whether this process is related to a physiological role remains unclear. Here, we explored the microbial manganese oxidation process under visible light by using coastal surface seawater microorganisms. Visible light greatly promotes the oxidation rate of Mn(II), and the average rate reaches 64 μmol/(L·d). The generated manganese oxides were then conducive to Mn(II) oxidation, thus the rapid manganese oxidation was the result of the combined action of biotic and abiotic, and biological function accounts for 88 % ± 4 %. Extracellular superoxide produced by microorganisms induced by visible light is the decisive factor for the rapid manganese oxidation in our study. But the production of these superoxides does not require the presence of Mn(II) ions, the Mn(II) oxidation process was more like an unintentional side reaction, which did not affect the growth of microorganisms. More than 70 % of heterotrophic microorganisms in nature are capable of producing superoxide, based on the oxidizing properties of free radicals, all these bacteria can participate in the geochemical cycle of manganese. What’s more, the superoxide oxidation pathway might be a significant natural source of manganese oxide.
P F Andeer, D R Learman, M McIlvin, J A Dunn, C M Hansel. (2015). Extracellular haem peroxidases mediate Mn(II) oxidation in a marine Roseobacter bacterium via superoxide production. Environmental Microbiology, 17( 10): 3925– 3936 https://doi.org/10.1111/1462-2920.12893
pmid: 25923595
2
C R Anderson, H A Johnson, N Caputo, R E Davis, J W Torpey, B M Tebo. (2009). Mn(II) oxidation is catalyzed by heme peroxidases in “Aurantimonas manganoxydans” strain SI85-9A1 and Erythrobacter sp. strain SD-21. Applied and Environmental Microbiology, 75( 12): 4130– 4138 https://doi.org/10.1128/AEM.02890-08
pmid: 19411418
3
M L Bender, G P Klinkhammer, D W Spencer. (1977). Manganese in seawater and the marine manganese balance. Deep-Sea Research, 24( 9): 799– 812 https://doi.org/10.1016/0146-6291(77)90473-8
4
E Cabiscol, J Tamarit, J Ros. (2000). Oxidative stress in bacteria and protein damage by reactive oxygen species. International Microbiology, 3( 1): 3– 8
pmid: 10963327
5
L Cabrol, M Quéméneur, B Misson. (2017). Inhibitory effects of sodium azide on microbial growth in experimental resuspension of marine sediment. Journal of Microbiological Methods, 133 : 62– 65 https://doi.org/10.1016/j.mimet.2016.12.021
pmid: 28039035
6
S K Carmichael S L Bräuer ( 2015) . Microbial diversity and manganese cycling: a review of manganese oxidizing microbial cave communities. In: Summers Engel A, ed. Microbial Life of Cave Systems. Berlin: De Gruyter
7
G Cebrián, S Condón, P Mañas. (2017). Physiology of the inactivation of vegetative bacteria by thermal treatments: mode of action, influence of environmental factors and inactivation kinetics. Foods, 6( 12): 107 https://doi.org/10.3390/foods6120107
pmid: 29189748
8
H Cui, B Li, Z Li, X Li, S Xu. (2018). Z-scheme based CdS/CdWO4 heterojunction visible light photocatalyst for dye degradation and hydrogen evolution. Applied Surface Science, 455 : 831– 840 https://doi.org/10.1016/j.apsusc.2018.06.054
9
J M Diaz, C M Hansel, B M Voelker, C M Mendes, P F Andeer, T Zhang. (2013). Widespread production of extracellular superoxide by heterotrophic bacteria. Science, 340( 6137): 1223– 1226 https://doi.org/10.1126/science.1237331
pmid: 23641059
10
R Ding, W Yan, Y Wu, Y Xiao, H Gang, S Wang, L Chen, F Zhao. (2018). Light-excited photoelectrons coupled with bio-photocatalysis enhanced the degradation efficiency of oxytetracycline. Water Research, 143 : 589– 598 https://doi.org/10.1016/j.watres.2018.06.068
pmid: 30015099
11
O W Duckworth, G Sposito. (2005). Siderophore-manganese(III) interactions. I. Air-oxidation of manganese(ll) promoted by desferrioxamine B. Environmental Science & Technology, 39( 16): 6037– 6044 https://doi.org/10.1021/es050275k
pmid: 16173561
12
I Forrez, M Carballa, K Verbeken, L Vanhaecke, M Schlüsener, T Ternes, N Boon, W Verstraete. (2010). Diclofenac oxidation by biogenic manganese oxides. Environmental Science & Technology, 44( 9): 3449– 3454 https://doi.org/10.1021/es9027327
pmid: 20369877
13
K Geszvain, L Smesrud, B M Tebo. (2016). Identification of a third Mn (II) oxidase enzyme in Pseudomonas putida GB-1. Applied and Environmental Microbiology, 82( 13): 3774– 3782 https://doi.org/10.1128/AEM.00046-16
pmid: 27084014
14
F D Halstead, J E Thwaite, R Burt, T R Laws, M Raguse, R Moeller, M A Webber, B A Oppenheim. (2016). Antibacterial activity of blue light against nosocomial wound pathogens growing planktonically and as mature biofilms. Applied and Environmental Microbiology, 82( 13): 4006– 4016 https://doi.org/10.1128/AEM.00756-16
pmid: 27129967
15
S P Hansard, H D Easter, B M Voelker. (2011). Rapid reaction of nanomolar Mn(II) with superoxide radical in seawater and simulated freshwater. Environmental Science & Technology, 45( 7): 2811– 2817 https://doi.org/10.1021/es104014s
pmid: 21375329
C M Hansel, C A Zeiner, C M Santelli, S M Webb. (2012). Mn(II) oxidation by an ascomycete fungus is linked to superoxide production during asexual reproduction. Proceedings of the National Academy of Sciences of the United States of America, 109( 31): 12621– 12625 https://doi.org/10.1073/pnas.1203885109
pmid: 22802654
H Hou, H Liu, F Gao, M Shang, L Wang, L Xu, W Wong, W Yang. (2018). Packaging BiVO4 nanoparticles in ZnO microbelts for efficient photoelectrochemical hydrogen production. Electrochimica Acta, 283 : 497– 508 https://doi.org/10.1016/j.electacta.2018.06.148
20
J Huang, H Zhang. (2020). Redox reactions of iron and manganese oxides in complex systems. Frontiers of Environmental Science & Engineering, 14( 5): 76 https://doi.org/10.1007/s11783-020-1255-8
21
H Jung, M Taillefert, J Sun, Q Wang, O J Borkiewicz, P Liu, L Yang, S Chen, H Chen, Y Tang. (2020). Redox cycling driven transformation of layered manganese oxides to tunnel structures. Journal of the American Chemical Society, 142( 5): 2506– 2513 https://doi.org/10.1021/jacs.9b12266
pmid: 31913621
22
M Koblížek, O Béjà, R R Bidigare, S Christensen, B Benitez-Nelson, C Vetriani, M K Kolber, P G Falkowski, Z S Kolber. (2003). Isolation and characterization of Erythrobacter sp. strains from the upper ocean. Archives of Microbiology, 180( 5): 327– 338 https://doi.org/10.1007/s00203-003-0596-6
pmid: 14504692
23
A Kumar, V Ghate, M J Kim, W Zhou, G H Khoo, H G Yuk. (2016). Antibacterial efficacy of 405, 460 and 520 nm light emitting diodes on Lactobacillus plantarum, Staphylococcus aureus and Vibrio parahaemolyticus. Journal of Applied Microbiology, 120( 1): 49– 56 https://doi.org/10.1111/jam.12975
pmid: 26481103
24
D R Learman, B M Voelker, A S Madden, C M Hansel. (2013). Constraints on superoxide mediated formation of manganese oxides. Frontiers in Microbiology, 4 : 262 https://doi.org/10.3389/fmicb.2013.00262
pmid: 24027565
25
D R Learman, B M Voelker, A I Vazquez-Rodriguez, C M Hansel. (2011). Formation of manganese oxides by bacterially generated superoxide. Nature Geoscience, 4( 2): 95– 98 https://doi.org/10.1038/ngeo1055
26
Y Li, L Chen, X Tian, L Lin, R Ding, W Yan, F Zhao. (2021). Functional role of mixed-culture microbe in photocatalysis coupled with biodegradation: Total organic carbon removal of ciprofloxacin. Science of the Total Environment, 784 : 147049 https://doi.org/10.1016/j.scitotenv.2021.147049
pmid: 34088071
27
J J Morris, A L Rose, Z Lu. (2022). Reactive oxygen species in the world ocean and their impacts on marine ecosystems. Redox Biology, 52 : 102285 https://doi.org/10.1016/j.redox.2022.102285
pmid: 35364435
28
K J Murray, S M Webb, J R Bargar, B M Tebo. (2007). Indirect oxidation of Co(II) in the presence of the marine Mn(II)-oxidizing bacterium Bacillus sp. strain SG-1. Applied and Environmental Microbiology, 73( 21): 6905– 6909 https://doi.org/10.1128/AEM.00971-07
pmid: 17827312
29
K Nakama, M Medina, A Lien, J Ruggieri, K Collins, H A Johnson. (2014). Heterologous expression and characterization of the manganese-oxidizing protein from Erythrobacter sp. strain SD21. Applied and Environmental Microbiology, 80( 21): 6837– 6842 https://doi.org/10.1128/AEM.01873-14
pmid: 25172859
30
K H (2006) Nealson. Volume 5: Proteobacteria: Alpha and Beta Subclasses. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K H, Stackebrandt E, editors. The Prokaryotes. New York: Springer, 222– 231
31
Nesbitt H W, Banerjee D (1998). Interpretation of XPS Mn(2p) spectra of Mn oxyhydroxides and constraints on the mechanism of MnO2 precipitation. American Mineralogist, 83(3–4): 305–315
32
P S Nico, C Anastasio, R J Zasoski. (2002). Rapid photo-oxidation of Mn(II) mediated by humic substances. Geochimica et Cosmochimica Acta, 66( 23): 4047– 4056 https://doi.org/10.1016/S0016-7037(02)01001-3
33
C Palermo, M Dittrich. (2016). Evidence for the biogenic origin of manganese-enriched layers in Lake Superior sediments. Environmental Microbiology Reports, 8( 2): 179– 186 https://doi.org/10.1111/1758-2229.12364
pmid: 26636960
34
P S Queiroz, F A D Ruas, N R Barboza, Castro Borges W de, R Guerra-Sá. (2018). Alterations in the proteomic composition of Serratia marcescens in response to manganese (II). BMC Biotechnology, 18( 1): 83 https://doi.org/10.1186/s12896-018-0493-3
pmid: 30594179
35
G Ramadoss, S P Suriyaraj, R Sivaramakrishnan, A Pugazhendhi, S Rajendran. (2021). Mesoporous ferromagnetic manganese ferrite nanoparticles for enhanced visible light mineralization of azoic dye into nontoxic by-products. Science of the Total Environment, 765 : 142707 https://doi.org/10.1016/j.scitotenv.2020.142707
pmid: 33069475
36
L L Richardson, C Aguilar, K H Nealson. (1988). Manganese oxidation in pH and O2 microenvironments produced by phytoplankton. Limnology and Oceanography, 33( 3): 352– 363 https://doi.org/10.4319/lo.1988.33.3.0352
pmid: 11538363
37
Y Song, J Jiang, J Ma, Y Zhou, U von Gunten. (2019). Enhanced transformation of sulfonamide antibiotics by manganese(IV) oxide in the presence of model humic constituents. Water Research, 153 : 200– 207 https://doi.org/10.1016/j.watres.2019.01.011
pmid: 30716563
38
Y Shi, Y Dai, Z Liu, X Nie, S Zhao, C Zhang, H Jia. (2020). Light-induced variation in environmentally persistent free radicals and the generation of reactive radical species in humic substances. Frontiers of Environmental Science & Engineering, 14( 6): 106
39
K M Sutherland, A Coe, R J Gast, S Plummer, C P Suffridge, J M Diaz, J S Bowman, S D Wankel, C M Hansel. (2019). Extracellular superoxide production by key microbes in the global ocean. Limnology and Oceanography, 64( 6): 2679– 2693 https://doi.org/10.1002/lno.11247
40
K M Sutherland, S D Wankel, C M Hansel. (2020). Dark biological superoxide production as a significant flux and sink of marine dissolved oxygen. Proceedings of the National Academy of Sciences of the United States of America, 117( 7): 3433– 3439 https://doi.org/10.1073/pnas.1912313117
pmid: 32015131
41
M Tardu, S Bulut, I H Kavakli. (2017). MerR and ChrR mediate blue light induced photo-oxidative stress response at the transcriptional level in Vibrio cholerae. Scientific Reports, 7( 1): 40817 https://doi.org/10.1038/srep40817
pmid: 28098242
42
B M Tebo, J R Bargar, B G Clement, G J Dick, K J Murray, D Parker, R Verity, S M Webb. (2004). Biogenic manganese oxides: properties and mechanisms of formation. Annual Review of Earth and Planetary Sciences, 32( 1): 287– 328 https://doi.org/10.1146/annurev.earth.32.101802.120213
43
B M Tebo, H A Johnson, J K McCarthy, A S Templeton. (2005). Geomicrobiology of manganese(II) oxidation. Trends in Microbiology, 13( 9): 421– 428 https://doi.org/10.1016/j.tim.2005.07.009
pmid: 16054815
44
C Tournassat, L Charlet, D Bosbach, A Manceau. (2002). Arsenic(III) oxidation by birnessite and precipitation of manganese(II) arsenate. Environmental Science & Technology, 36( 3): 493– 500 https://doi.org/10.1021/es0109500
pmid: 11871566
45
L Wu, G Zhu, X Zhang, Y Si. (2020). Silver nanoparticles inhibit denitrification by altering the viability and metabolic activity of Pseudomonas stutzeri. Science of the Total Environment, 706 : 135711 https://doi.org/10.1016/j.scitotenv.2019.135711
pmid: 31791784
46
W Xia, R Chen, Y Li, P Gao, C Li, T Jin, J Ma, T Ma. (2021). Photo-driven heterogeneous microbial consortium reducing CO2 to hydrocarbons fuel. Journal of Cleaner Production, 326 : 129397 https://doi.org/10.1016/j.jclepro.2021.129397
47
J Xu, M Zhao, L Pei, X Liu, L Wei, A Li, Y Mei, Q Xu. (2020). Effects of heavy metal mixture exposure on hematological and biomedical parameters mediated by oxidative stress. Science of the Total Environment, 705 : 134865 https://doi.org/10.1016/j.scitotenv.2019.134865
48
X Xu, Y Li, Y Li, A Lu, R Qiao, K Liu, H Ding, C Wang. (2019). Characteristics of desert varnish from nanometer to micrometer scale: a photo-oxidation model on its formation. Chemical Geology, 522 : 55– 70 https://doi.org/10.1016/j.chemgeo.2019.05.016
49
F Yang, Y Zheng, X Tian, Y Liu, J Li, Z Shao, F Zhao. (2021). Redox cycling of manganese by Bacillus horikoshii biET1 via oxygen switch. Electrochimica Acta, 375 : 137963 https://doi.org/10.1016/j.electacta.2021.137963
50
G Yang, W Ni, K Wu, H Wang, B E Yang, X Jia, R Jin. (2013). The effect of Cu(II) stress on the activity, performance and recovery on the Anaerobic Ammonium-Oxidizing (Anammox) process. Chemical Engineering Journal, 226 : 39– 45 https://doi.org/10.1016/j.cej.2013.04.019
51
X Yang, Q Peng, L Liu, W Tan, G Qiu, C Liu, Z Dang. (2020). Synergistic adsorption of Cd(II) and As(V) on birnessite under electrochemical control. Chemosphere, 247 : 125822 https://doi.org/10.1016/j.chemosphere.2020.125822
pmid: 31927232
52
T Zhang, L Liu, W Tan, S L Suib, G Qiu, F Liu. (2018). Photochemical formation and transformation of birnessite: effects of cations on micromorphology and crystal structure. Environmental Science & Technology, 52( 12): 6864– 6871 https://doi.org/10.1021/acs.est.7b06592
pmid: 29792324
53
H Zhao, Y Wang, Y Liu, K Yin, D Wang, B Li, H Yu, M Xing. (2021). ROS-induced hepatotoxicity under cypermethrin: involvement of the crosstalk between Nrf2/Keap1 and NF-kappaB/ikappaB-alpha pathways regulated by proteasome. Environmental Science & Technology, 55( 9): 6171– 6183 https://doi.org/10.1021/acs.est.1c00515
pmid: 33843202
54
Y Zheng, A Kappler, Y Xiao, F Yang, G D Mahadeva, F Zhao. (2019). Redox-active humics support interspecies syntrophy and shift microbial community. Science China Technological Sciences, 62( 10): 1695– 1702 https://doi.org/10.1007/s11431-018-9360-5
55
H Zhou, C Fu. (2020). Manganese-oxidizing microbes and biogenic manganese oxides: characterization, Mn(II) oxidation mechanism and environmental relevance. Reviews in Environmental Science and Biotechnology, 19( 3): 489– 507 https://doi.org/10.1007/s11157-020-09541-1
