Natural mineral photoelectric effect: non-classical mineral photosynthesis

doi:10.13745/j.esf.sf.2020.5.35

Abstract

Abstract:

Under the ever-existing solar irradiation, the organisms on Earth have evolved with a structurally sophisticated photosynthesis system. However, the inherent impact and response mechanism of solar illumination on the inorganic minerals widespread on the Earth surface has drawn little attention. We discovered for the first time the solar energy conversion system of the “mineral membrane”, which exerts potential oxygen production and carbon sequestration functions on the Earth surface. Our finding shed light on the photoelectric effect and non-classical photosynthesis of the natural semiconducting minerals. We carried out this research on the semiconducting property and photoelectron energy of the typical minerals in the “mineral membrane”. We further discussed the photoelectric effect, oxygen production and carbon sequestration functions of the ferromanganese oxides, as well as the corresponding geological records. We proposed that the sensitive and stable photon-to-electron conversion are performed by birnessite, goethite and hematite, which are semiconducting minerals commonly present in the natural “mineral membrane”. In addition, we put forward the non-classical mineral photosynthesis function as follows: the solar energy conversion system developed by inorganic minerals resembles the biological photosynthesis process regarding to oxygen evolving and carbon fixing; also, the “mineral membrane” may take part in the photocatalytic water-oxidation reaction and in the transformation of atmospheric CO₂ into marine carbonate. Last but not least, minerals might as well have promoted the biologic photosynthesis system as the core complex in the Mn₄CaO₅ photosynthesis system evolved during water-oxidation process to form the structural analog birnessite. Therefore, it is fair to postulate that birnessite could play a role in the initiation of the photosynthesis system of cyanobacteria. On the other hand, minerals could weaken hydrogen bond strength and alter water property, thus to facilitate water oxidation and photosynthesis efficiencies, which would hopefully give further insights into the molecular mechanism of mineral participation in the biologic photosynthesis process.

Key words: mineral photoelectric effect, mineral non-classical photosynthesis, birnessite, mineral photoelectron energy, oxygen production and carbon sequestration

CLC Number:

P574
P571

LU Anhuai, LI Yan, DING Hongrui, WANG Changqiu, XU Xiaoming, LIU Feifei, LIU Yuwei, ZHU Ying, LI Yanzhang. Natural mineral photoelectric effect: non-classical mineral photosynthesis[J]. Earth Science Frontiers, 2020, 27(5): 179-194.

Figures/Tables 9

Fig.1 Three significant energy carriers in nature: solar photons, mineralphotoelectrons and elemental valence electrons. Adapted from [2].

Fig.2 A schematic diagram of the natural photosynthesis process, noting the “new sphere” of the “mineral membrane” as the topmost layer of the Earth surface. Adapted from [6].

Fig.3 In-situ, sensitive and stable photocurrent produced by the “mineral membrane”. Adapted from [3].

Fig.4 Structural and functional comparisons of Mn4CaO5 in the natural and artificial photosynthesis processes. Adapted from [28].

Fig.5 Five different phases of the catalytic oxygen-evolving-centers (OEC). Adapted from [28,30].

Fig.6 Structural transformation of Mn4CaO5 during biologic photosynthesis-II and oxygen-evolving process. Adapted from [39].

Table 1 Comparison of oxygen production mechanisms of birnessite and biologic photosynthesis-II. Adapted from [39].

光反应部位	催化状态	产氧过程
生物PSⅡ	S₁-S₃	Mn(Ⅲ)逐步被氧化
水钠锰矿	S₁-S₄	Mn(Ⅲ)逐步被氧化
生物PSⅡ	S₄	形成O—O键
水钠锰矿	S₅	形成O—O键
生物PSⅡ	S₄-S₀-S₁	Mn(Ⅳ)被还原,H₂O被氧化,释放O₂
水钠锰矿	S₅-S₆-S₁	Mn(Ⅳ)被还原,H₂O被氧化,释放O₂

Fig.7 Birnessite phases produced in the [Mn4O4L6]+ catalytic oxygen-evolving process: (a) [Mn4O4L6]+ catalytic oxygen-evolving process; (b) Manganese K-edge EXAFS spectra of products. Adapted form [33].

Fig.8 Transformation mechanism of CO2 to carbonate minerals by birnessite in soil. Adapted from [54].

References 92

[1]	鲁安怀, 李艳, 王鑫, 等. 关键带中天然半导体矿物光电子的产生与作用[J]. 地学前缘, 2014, 21(3):256-264.
[2]	鲁安怀, 李艳, 丁竑瑞, 等. 矿物光电子能量及矿物与微生物协同作用[J]. 矿物岩石地球化学通报, 2018, 37(1):1-15.
[3]	LU A, Li Y, DING H, et al. Photoelectric conversion on Earth’s surface via widespread Fe-and Mn-mineral coatings[J]. Proceedings of the National Academy of Sciences, 2019, 116(20):9741-9746. DOI URL
[4]	SHUEY R. Semiconducting ore minerals[M]. Amsterdam: Elsevier, 1975.
[5]	VAUGHAN D, CRAIG J. Mineral chemistry of metal sulfides[M]. Cambridge: Cambridge University Press, 1978.
[6]	鲁安怀, 李艳, 丁竑瑞, 等. 地表“矿物膜”: 地球“新圈层”[J]. 岩石学报, 2019, 35(1):119-128.
[7]	ENGEL C G, SHARP R P. Chemical data on desert varnish[J]. Geological Society of America Bulletin, 1958, 69:273-286.
[8]	DORN R I, OBERLANDER T M. Microbial origin of desert varnish[J]. Science, 1981, 213:1245.
[9]	DORN R I, DENIRO M J. Stable carbon isotope ratios of rock varnish organic matter: a new paleoenvironmental indicator[J]. Science, 1985, 227:1472-1474.
[10]	DORN R I. Rock varnish[J]. American Scientist, 1991, 79:542-553.
[11]	DIGREGORIO B E. Rock varnish as a habitat for extant life on Mars[M]// HOOVER R B, LEVIN G V, PAEPE R R, et al. Instruments, methods, and missions for astrobiology Ⅳ. San Diego, California, USA: International Society for Optics and Photonics, 2001: 120-130.
[12]	PERRY R S, KOLB V M. From Darwin to Mars: desert varnish as a model for preservation of complex (bio)chemical systems[J]. SPIE International Symposium on Optical Science and Technology, 2004, 5163:136-144.
[13]	LANZA N L, CLEGG S M, WIENS R C, et al. Examining natural rock varnish and weathering rinds with laser-induced breakdown spectroscopy for application to ChemCam on Mars[J]. Applied Optics, 2012, 51:B74-B82.
[14]	GAO S, LUO T C, ZHANG B R, et al. Chemical composition of the continental curst as revealed by studies in east China[J]. Geochimica et Cosmochimica Acta, 1998, 62:1959-1975.
[15]	XU X, DING H, LI Y, et al. Mineralogical characteristics of Mn coatings from different weathering environments in China: clues on their formation[J]. Mineralogy and Petrology, 2018, 112:671-683.
[16]	XU X, LI Y, LI Y, et al. Characteristics of desert varnish from nanometer to micrometer scale: a photo-oxidation model on its formation[J]. Chemical Geology, 2019, 522:55-70. DOI URL
[17]	POTTER R M, ROSSMAN G R. The manganese- and iron-oxide mineralogy of desert varnish[J]. Chemical Geology, 1979, 25:79-94. DOI URL
[18]	MCKEOWN D A, POST J E. Characterization of manganese oxide mineralogy in rock varnish and dendrites using X-ray absorption spectroscopy[J]. American Mineralogist, 2001, 86:701-713. DOI URL
[19]	GARVIE L A J, BURT D M, BUSECK P R. Nanometer-scale complexity, growth, and diagenesis in desert varnish[J]. Geology, 2008, 36:215-218.
[20]	THIAGARAJAN N, LEE C T A. Trace-element evidence for the origin of desert varnish by direct aqueous atmospheric deposition[J]. Earth and Planetary Science Letters, 2004, 224:131-141.
[21]	GOLDSMITH Y, STEIN M, ENZEL Y. From dust to varnish: geochemical constraints on rock varnish formation in the Negev Desert, Israel[J]. Geochimica et Cosmochimica Acta, 2014, 126:97-111.
[22]	POST J E. Manganese oxide minerals: crystal structures and economic and environmental significance[J]. Proceedings of the National Academy of Sciences, 1999, 96:3447-3454. DOI URL
[23]	RUALES-LONFAT C, BARONA J F, SIENKIWICZ A, et al. Iron oxides semiconductors are efficients for solar water disinfection: a comparison with photo-Fenton processes at neutral pH[J]. Applied Catalysis B: Environmental, 2015, 166:497-508.
[24]	PINAUD B A, CHEN Z, ABRAM D N, et al. Thin films of sodium birnessite-type MnO₂: optical properties, electronic band structure, and solar photoelectrochemistry[J]. The Journal of Physical Chemistry C, 2011, 115(23):11830-11838. DOI URL
[25]	LUCHT K P, MENDOZA-CORTES J L. Birnessite: a layered manganese oxide to capture sunlight for water-splitting catalysis[J]. The Journal of Physical Chemistry C, 2015, 119(40):22838-22846. DOI URL
[26]	UMENA Y, KAWAKAMI K, SHEN J R, et al. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å[J]. Nature, 2011, 473(7345):55-60. DOI URL
[27]	SUGA M, AKITA F, HIRATA K, et al. Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses[J]. Nature, 2015, 517(7532):99-103. DOI URL
[28]	ZHANG C, CHEN C, DONG H, et al. A synthetic Mn₄Ca-cluster mimicking the oxygen-evolving center of photosynjournal[J]. Science, 2015, 348(6235):690-693. DOI URL
[29]	DAU H, HAUMANN M. The manganese complex of photosystem II in its reaction cycle: basic framework and possible realization at the atomic level[J]. Coordination Chemistry Reviews, 2008, 252(3/4):273-295. DOI URL
[30]	COX N, PANTAZIS D A, NEESE F, et al. Biological water oxidation[J]. Accounts of Chemical Research, 2013, 46(7):1588-1596. DOI URL
[31]	JONES L H P, MILNE A A. Birnessite, a new manganese oxide mineral from Aberdeenshire, Scotland[J]. Mineralogical Magazine, 1956, 31:283-288.
[32]	HSU Y K, CHEN Y C, LIN Y G, et al. Birnessite-type manganese oxides nanosheets with hole acceptor assisted photoelectrochemical activity in response to visible light[J]. Journal of Materials Chemistry, 2012, 22(6):2733-2739. DOI URL
[33]	HOCKING R K, BRIMBLECOMBE R, CHANG L Y, et al. Water-oxidation catalysis by manganese in a geochemical-like cycle[J]. Nature Chemistry, 2011, 3(6):461-466.
[34]	GORLIN Y, LASSALLE-KAISER B, BENCK J D, et al. In situ X-ray absorption spectroscopy investigation of a bifunctional manganese oxide catalyst with high activity for electrochemical water oxidation and oxygen reduction[J]. Journal of the American Chemistry Society, 2013, 135:8525-8534. DOI URL
[35]	PENG H, MCKENDRY I G, DING R, et al. Redox properties of birnessite from a defect perspective[J]. Proceedings of the National Academy of Sciences, 2017, 114(36):9523-9528. DOI URL
[36]	WIECHEN M, ZAHARIEVA I, DAU H, et al. Layered manganese oxides for water-oxidation: alkaline earth cations influence catalytic activity in a photosystem II-like fashion[J]. Chemical Science, 2012, 3(7):2330-2339. DOI URL
[37]	FREY C E, WIECHEN M, KURZ P. Water-oxidation catalysis by synthetic manganese oxides: systematic variations of the calcium birnessite theme[J]. Dalton Transactions, 2014, 43(11):4370-4379. DOI URL
[38]	TAKAHASHI Y, MANCEAU A, GEOFFROY N, et al. Chemical and structural control of the partitioning of Co, Ce, and Pb in marine ferromanganese oxides[J]. Geochimica et Cosmochimica Acta, 2007, 71(4):984-1008. DOI URL
[39]	YANG J, AN H, ZHOU X, et al. Water oxidation mechanism on alkaline-earth-cation containing birnessite-like manganese oxides[J]. The Journal of Physical Chemistry C, 2015, 119(32):18487-18494.
[40]	LYONST W, REINHARD C T, PLANAVSKY N J. The rise of oxygen in Earth’s early ocean andatmosphere[J]. Nature, 2014, 506(7488):307-315.
[41]	KENNEDY M J, PEVEAR D R, HILL R J. Mineral surface control of organic carbon in black shale[J]. Science, 2002, 295(5555):657-660. DOI URL
[42]	KENNEDY M, DROSER M, MAYER L M, et al. Late Precambrian oxygenation: inception of the clay mineral factory[J]. Science, 2006, 311(5766):1446-1449. DOI URL
[43]	CAMPBELL I H, ALLEN C M. Formation of supercontinents linked to increases in atmospheric oxygen[J]. Nature Geosciences, 2008, 1:554-558. DOI URL
[44]	SQUIRE R J, CAMPBELL I H, ALLEN C M, et al. Did the Transgondwanan Supermountain trigger the explosive radiation of animals on Earth?[J]. Earth and Planetary Science Letters, 2006, 250(1/2):116-133. DOI URL
[45]	LINDSAY J F, BRASIER M D. Did global tectonics drive early biosphere evolution? Carbon isotope record from 2.6 to 1.9 Ga carbonates of Western Australian basins[J]. Precambrian Research, 2002, 114:1-34. DOI URL
[46]	CANFIELD D E. The early history of atmospheric oxygen: Homage to Robert M. Garrels[J]. Annual Review of Earth and Planetary Science, 2005, 33:1-36. DOI URL
[47]	CAMPBELL I H, SQUIRE R J. The mountains that triggered the Late Neoproterozoic increase in oxygen: the second great oxidation event[J]. Geochimica et Cosmochimica Acta, 2010, 74:4187-4206. DOI URL
[48]	BERNER R A. GEOCARBSULF: a combined model for Phanerozoic atmospheric O₂ and CO₂[J]. Geochimica et Cosmochimica Acta, 2006, 70:5653-5664. DOI URL
[49]	MATTE P. The Variscan collage and orogeny (480-290 Ma) and the tectonic definition of the Armorica microplate: a review[J]. Terra Nova, 2001, 13:122-128.
[50]	BROCKS J J, BUICK R, SUMMONS R E, et al. A reconstruction of Archean biological diversity based on molecular fossils from the 2.78 to 2.45 billion-year-old Mount Bruce Supergroup, Hamersley Basin, Western Australia[J]. Geochimica et Cosmochimica Acta, 2003, 67(22):4321-4335. DOI URL
[51]	SUMMONS R E, BRADLEY A S, JAHNKE L L, et al. Steroids, triterpenoids and molecular oxygen[J]. Philosophical Transactions of the Royal Society B: Biological Sciences, 2006, 361(1470):951-968.
[52]	ZHANG X V, ELLERY S P, FRIEND C M, et al. Photodriven reduction and oxidation reactions on colloidal semiconductor particles: implications for prebiotic synjournal[J]. Journal of Photochemistry and Photobiology A: Chemistry, 2007, 185(2/3):301-311.
[53]	LU A, LI Y, JIN S, et al. Growth of non-phototrophic microorganisms using solar energy through mineral photocatalysis[J]. Nature Communications, 2012, 3(1):1-8.
[54]	LI Y, WANG X, LI Y, et al. Coupled anaerobic and aerobic microbial processes for Mn-carbonate precipitation: a realistic model of inorganic carbon pool formation[J]. Geochimica et Cosmochimica Acta, 2019, 256:49-65. DOI URL
[55]	ALLWOOD A C, WALTER M R, KAMBER B S, et al. Stromatolite reef from the Early Archaean era of Australia[J]. Nature, 2006, 441(7094):714-718. DOI URL
[56]	DUPRAZ C, VISSCHER P T. Microbial lithification in marine stromatolites and hypersaline mats[J]. Trends in Microbiology, 2005, 13(9):429-438. DOI URL
[57]	王艺凝, 刘建波, 足立奈津子, 等. 华南上扬子台地南缘早奥陶世生物礁演变规律及其控制因素[C]// 中国古生物学会第十二次全国会员代表大会暨第29届学术年会摘要集. 郑州: 中国古生物学会, 2018: 44.
[58]	VASCONCELOS C, MCKENZIE J A, BERNASCONI S, et al. Microbial mediation as a possible mechanism for natural dolomite formation at low temperatures[J]. Nature, 1995, 377(6546):220-222. DOI URL
[59]	VASCONCELOS C, MCKENZIE J A. Microbial mediation of modern dolomite precipitation and diagenesis under anoxic conditions (Lagoa Vermelha, Rio de Janeiro, Brazil)[J]. Journal of Sedimentary Research, 1997, 67(3):378-390.
[60]	WARTHMANN R, VAN LITH Y, VASCONCELOS C, et al. Bacterially induced dolomite precipitation in anoxic culture experiments[J]. Geology, 2000, 28(12):1091-1094. DOI URL
[61]	VAN LITH Y, WARTHMANN R, VASCONCELOS C, et al. Sulphate-reducing bacteria induce low-temperature Ca-dolomite and high Mg-calcite formation[J]. Geobiology, 2003, 1(1):71-79. DOI URL
[62]	BEVERIDGE T J. Role of cellular design in bacterial metal accumulation and mineralization[J]. Annual Review of Microbiology, 1989, 43(1):147-171. DOI URL
[63]	FOLK R L. SEM imaging of bacteria and nannobacteria in carbonate sediments and rocks[J]. Journal of Sedimentary Research, 1993, 63(5):990-999.
[64]	WACEY D, WRIGHT D T, BOYCE A J. A stable isotope study of microbial dolomite formation in the Coorong Region, South Australia[J]. Chemical Geology, 2007, 244(1/2):155-174. DOI URL
[65]	WRIGHT D T. The role of sulphate-reducing bacteria and cyanobacteria in dolomite formation in distal ephemeral lakes of the Coorong region, South Australia[J]. Sedimentary Geology, 1999, 126(1/2/3/4):147-157. DOI URL
[66]	WACEY D. Microbial mediation of dolomite formation: geochemical and microbial investigations in the Coorong region of South Australia[D]. London: University of Oxford, 2002.
[67]	WRIGHT D T, WACEY D. Sedimentary dolomite: a reality check[J]. Geological Society, London, Special Publications, 2004, 235(1):65-74.
[68]	ZHANG F, XU H, KONISHI H, et al. Dissolved sulfide-catalyzed precipitation of disordered dolomite: implications for the formation mechanism of sedimentary dolomite[J]. Geochimica et Cosmochimica Acta, 2012, 97:148-165. DOI URL
[69]	ZHANG F, XU H, KONISHI H, et al. Polysaccharide-catalyzed nucleation and growth of disordered dolomite: a potential precursor of sedimentary dolomite[J]. American Mineralogist, 2012, 97(4):556-567.
[70]	NOFFKE N. The criteria for the biogeneicity of microbially induced sedimentary structures (MISS) in Archean and younger, sandy deposits[J]. Earth-Science Reviews, 2009, 96(3):173-180. DOI URL
[71]	MCKENZIE J A, VASCONCELOS C. Dolomite Mountains and the origin of the dolomite rock of which they mainly consist: historical developments and new perspectives[J]. Sedimentology, 2009, 56(1):205-219. DOI URL
[72]	PETRASH D A, BIALIK O M, BONTOGNALI T R R, et al. Microbially catalyzed dolomite formation: from near-surface to burial[J]. Earth-Science Reviews, 2017, 171:558-582.
[73]	KENARD P A, GONZALEZ L A, GOLDSTEIN R H, et al. Impact of biogenic methane generation on formation of dolomite reservoirs[C]// Proceedings of AAPG Annual Convention. 2007: 90063.
[74]	KENWARD P A, GOLDSTEIN R H, GONZALEZ L A, et al. Precipitation of low-temperature dolomite from an anaerobic microbial consortium: the role of methanogenic Archaea[J]. Geobiology, 2009, 7(5):556-565. DOI URL
[75]	SAUER K, YACHANDRA V K. A possible evolutionary origin for the Mn₄ cluster of the photosynthetic water oxidation complex from natural MnO₂ precipitates in the early ocean[J]. Proceedings of the National Academy of Sciences, 2002, 99:8631-8636.
[76]	FISCHER W W, KNOLL A H. An iron shuttle for deepwater silica in late Archean and early Paleoproterozoic iron formation[J]. Geological Society of American Bulletin, 2009, 121(1/2):222-235.
[77]	BEUKES N, KLEIN C. Models for iron-formation deposition. The Proterozoic biosphere: a multidisciplinary study[M]. Cambridge: Cambridge University Press, 1992: 147-156.
[78]	CLEMENT B G, LUTHER G W III, TEBO B M. Rapid, oxygen-dependent microbial Mn(Ⅱ) oxidation kinetics at sub-micromolar oxygen concentrations in the Black Sea suboxic zone[J]. Geochimica et Cosmochimica Acta, 2009, 73(7):1878-1889. DOI URL
[79]	KOPP R E, KIRSCHVINK J L, HILBURN I A, et al. The Paleoproterozoic snowball Earth: a climate disaster triggered by the evolution of oxygenic photosynthesis[J]. Proceedings of the National Academy of Sciences, 2005, 102(32):11131-11136.
[80]	HOLLAND H D. The oxygenation of the atmosphere and oceans[J]. Philosophical Transactions of the Royal Society B: Biological Sciences, 2006, 361(1470):903-915. DOI URL
[81]	JOHNSON J E, WEBB S M, THOMAS K, et al. Manganese-oxidizing photosynthesis before the rise of cyanobacteria[J]. Proceedings of the National Academy of Sciences, 2013, 110(28):11238-11243. DOI URL
[82]	DISMUKES G C, KLIMOV V V, BARANOV S V, et al. The origin of atmospheric oxygen on Earth: the innovation of oxygenic photosynthesis[J]. Proceedings of the National Academy of Sciences, 2001, 98(5):2170-2175. DOI URL
[83]	LU A, LI Y, WANG X, et al. Photoelectrons from minerals and microbial world: a perspective on life evolution in the early Earth[J]. Precambrian Research, 2013, 231:401-408. DOI URL
[84]	BRINI E, FENNELL C J, FERNANDEZ-SERRA M, et al. How water’s properties are encoded in its molecular structure and energies[J]. Chemical Reviews, 2017, 117(19):12385-12414. DOI URL
[85]	LARS G M, PETTERSSON R H, HENCHMAN A N. Water: the most anomalous liquid[J]. Chemical Reviews, 2016, 116:7459-7462. DOI URL
[86]	BERNAL J D, FOWLER R H. A theory of water and ionic solution, with particular reference to hydrogen and hydroxyl ions[J]. Journal of Chemistry Physics, 1933, 1:515-548. DOI URL
[87]	FREY P A, WHITT S A, TOBIN J B. A low-barrier hydrogen bond in the catalytic triad of serine proteases[J]. Science, 1994, 264(5167):1927-1930.
[88]	ZHANG C. Low-barrier hydrogen bond plays key role in active photosystem II: a new model for photosynthetic water oxidation[J]. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 2007, 1767(6):493-499. DOI URL
[89]	BAO H, ZHANG C, REN Y, et al. Low-temperature electron transfer suggests two types of QA in intact photosystem II[J]. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 2010, 1797(3):339-346. DOI URL
[90]	张纯喜. 从自然光合作用到人工光合作用[J]. 中国科学: 化学, 2016, 46(10):1101-1109.
[91]	赵国忠. 太赫兹科学技术研究的新进展[J]. 国外电子测量技术, 2014, 33(2):1-6.
[92]	范姝婷, 马莹玉, 舒国响, 等. 太赫兹与水的相互作用: 机理、应用和新趋势[J]. 深圳大学学报(理工版), 2019, 36(2):200-206.