Non-linear frequency-doubling up-conversion in sulfide minerals enables deep-sea oxygenic photosynthesis

Abstract

Visible light emission exceeding purely thermal radiation has been imaged at deep-sea hydrothermal vents, yet the underlying mechanisms remain unexplained. Here, we show that visible light can be produced from geothermal infrared radiation via nonlinear frequency-doubling up-conversion in sulfide minerals that are abundant in hydrothermal vents. Chalcopyrite exhibits significant second harmonic generation, which is further amplified under high pressure, yielding a 400-700 nm photon flux three orders of magnitude greater than blackbody emission. When exposed to 1064 nm of irradiation, chalcopyrite induces fluorescence responses in the cyanobacterium Synechococcus sp. PCC 7002 at 656 and 685 nm, suggesting that the up-converted 532 nm light is absorbed by phycobilisomes and transferred to photosystem II. Metagenomic analysis reveals a strong correlation between cyanobacteria and high-temperature, chalcopyrite-rich vents. Similar up-conversion processes have also been observed in other sulfide minerals, emitting wavelengths covering the entire visible spectrum. These findings unveil a novel mineral-mediated photonic mechanism that generates biologically relevant visible light at hydrothermal vents, which can be harnessed by oxygenic photosynthetic cyanobacteria in Earth's deep biosphere and possibly beyond.

Keywords: chalcopyrite; cyanobacteria; deep-sea hydrothermal system; oxygenic photosynthesis; second harmonic generation; sulfide mineral.

Figure 1.

Optical spectrum analysis of chalcopyrite from deep-sea hydrothermal vents. (a) Schematic diagram of frequency-doubling measurement on the deep-sea hydrothermal sulfides. Two photons at frequency ω interact with the sulfide sample and generate a new photon with a doubled frequency (2ω) and half the wavelength of the excitation light. (b) Emission spectra of sulfide minerals under a supercontinuum laser (800–1500 nm). Compared with the other four sulfides, the spectrum of chalcopyrite shows an obvious peak at ∼471 nm. (c) Excitation-power-dependent second harmonic generation (SHG) intensity in chalcopyrite. Under different excitation wavelengths, all three curves show the expected quadratic law. (d) Excitation power-dependent frequency-doubling conversion efficiency in chalcopyrite. The conversion efficiency increases linearly with the excitation light power, arriving at over ∼10⁻¹⁴ at 1.5 mW with 928 nm of excitation. (e) 2D photoluminescence spectrum of chalcopyrite showing a peak at ∼471 nm, consistent with that from the SHG spectrum in (c), indicating a special excitation state at ∼2.63 eV. (f) Emission spectra of chalcopyrite measured in a diamond anvil cell (DAC), showing increasing SHG intensity with hydrostatic pressure.

Figure 2.

Fluorescence response of cyanobacteria to infrared-irradiated sulfide minerals. (a) Schematic diagram of the fluorescence experiments. The wavelength of excitation laser (λ_ex) and the wavelength of SHG (λ_ex) is 1064 and 532 nm, respectively. The magnification of objective lens is denoted as ×50. (b) Emission spectrum of Synechococcus sp. PCC 7002 (7002) upon a chalcopyrite substrate irradiated by 1064 nm infrared light. (c) Fluorescence spectra of 7002 recorded on chalcopyrite (Cpy, curve with square). The fluorescence emission from 7002 on Cpy can be well fitted with three component peaks at 656, 685 and 713 nm, indicative of the up-converted light is absorbed by phycobilisome (PBS) and the excitation energy is transferred to photosystem II (PSII) and photosystem I (PSI). (d) Fluorescence spectra of 7002 recorded on glass (Glass, curve with circle) and galena (Gal, curve with triangle). No detectable fluorescence was observed when substituting Cpy with a glass or Gal substrate, or replacing 7002 with a sterile culture medium (A-plus, curve with diamond).

Figure 3.

Metagenomic analysis of photosynthesis-related genes in marine systems. (a) Diagram illustrating photosynthetic electron transfer and functional genes associated with the phototrophic apparatus, including Photosystem I, Photosystem II, cytochrome b₆f complex, photosynthetic electron transport, allophycocyanin (AP), phycocyanin (PC)/phycoerythrocyanin (PEC) and phycoerythrin (PE). (b) Completeness of functional genes related to the phototrophic apparatus of datasets across four marine environments. Metagenomic datasets are classified into: 27 from central region of deep-sea hydrothermal vents (C1, >350°C), 43 from central region of deep-sea hydrothermal vents (C2, <350°C), 30 from shallow hydrothermal deposits (S) and 42 from deep-sea locations distant from hydrothermal vents (N).

Figure 4.

Extensive visible emissions in hydrothermal sulfide minerals. (a) SHG emission spectra of five sulfide minerals overlapping with the absorption spectra of photosynthetic pigments (chlorophyll a: blue area, chlorophyll b: green area, carotenoids: yellow area). (b) Schematic illustrating the mineralogical mechanism that converts infrared light into visible light via SHG, thereby supporting photosynthetic microorganisms in the deep sea.