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Light-driven anaerobic microbial oxidation of manganese

Abstract

Oxygenic photosynthesis supplies organic carbon to the modern biosphere, but it is uncertain when this metabolism originated. It has previously been proposed1,2 that photosynthetic reaction centres capable of splitting water arose by about 3 billion years ago on the basis of the inferred presence of manganese oxides in Archaean sedimentary rocks. However, this assumes that manganese oxides can be produced only in the presence of molecular oxygen3, reactive oxygen species4,5 or by high-potential photosynthetic reaction centres6,7. Here we show that communities of anoxygenic photosynthetic microorganisms biomineralize manganese oxides in the absence of molecular oxygen and high-potential photosynthetic reaction centres. Microbial oxidation of Mn(ii) under strictly anaerobic conditions during the Archaean eon would have produced geochemical signals identical to those used to date the evolution of oxygenic photosynthesis before the Great Oxidation Event1,2. This light-dependent process may also produce manganese oxides in the photic zones of modern anoxic water bodies and sediments.

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Fig. 1: Biofilms incubated for two weeks.
Fig. 2: XRD spectra of biofilms incubated for two weeks.
Fig. 3: Interactions between minerals and microorganisms in biofilms incubated with Mn(ii) in the light for two weeks.

Data availability

Sequence data are available as FASTQ files at the National Center for Biotechnology Information (NCBI) via Sequence Read Archive (SRA), under the SRA accession number SRP133329. The datasets that support the findings of this study are available from the figshare repository (https://figshare.com/), with the identifiers 10.6084/m9.figshare.9738515, 10.6084/m9.figshare.9738725, 10.6084/m9.figshare.9738776, 10.6084/m9.figshare.9738905, 10.6084/m9.figshare.9738797, 10.6084/m9.figshare.9738878, 10.6084/m9.figshare.9738887, and 10.6084/m9.figshare.9738896. All other supporting data that support the findings of this study are available from the corresponding authors.

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Acknowledgements

We thank the current members of the Bosak laboratory, the Simons Foundation Collaboration on the Origins of Life (no. 327126 to T.B. and no. 339603 to G.F.), FESD NSF project (no. 1338810 to T.B.) and NSF Integrated Earth Systems (no. 1615426 to G.F. and T.B.). The NSF award number DMR-1419807 funded MIT Center for Material Science and Engineering (part of Materials Research Science and Engineering Center, NSF ECCS. award no. 1541959) funded the Harvard University Center for Nanoscale Systems (CNS), a member of the National Nanotechnology Coordinated Infrastructure Network (NNCI). The DOE Office of Science User Facility under contract no. DE-AC02-05CH11231 supports the Advanced Light Source and BI L12.3.2. M.P. and T.B. received funding from the John Templeton foundation, and M.P. was also supported by the Professor Amar G. Bose Research Grant Program (MIT).

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M.D. and T.B. conceived and designed the project. M.D. performed microbial enrichment experiments and analysed data. M.D. and N.T. performed synchrotron μXRD diffraction and analysed data. M.D. and M.P. performed oxygen concentration measurement experiments and analysed data. V.K.-C. and S.R. analysed the composition of microbial communities and performed bioinformatics analyses. V.K.-C. and A.F.-S. conducted bioinformatics analyses of the co-cultures and pure culture genomes. G.F. wrote about the molecular evolution of photosynthetic groups and contributed Extended Data Fig. 6. N.B. contributed to the writing by commenting on Archaean geology. M.D. and T.B. wrote the manuscript with input from M.P. and V.K.-C., N.B. and G.F. All co-authors reviewed and approved the final manuscript.

Corresponding authors

Correspondence to Mirna Daye or Tanja Bosak.

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Extended data figures and tables

Extended Data Fig. 1 Partial pressure of oxygen in the headspace of enrichment cultures and dark controls.

Oxygen concentration (μatm) measured in the headspaces of 150-ml serum bottles that contained 100 ml of MFGL medium, 50 μM sulfide and 1 mM MnCl2. One inoculated culture was incubated in the light (red points) and another in the dark (blue points). The sterile control (green points) was incubated in the light. Individual points are measurements by the oxygen sensor taken every 48.2 s. To control for sensor drift and recalibrate the zero point of the sensor, the bottles were flushed with oxygen-free N2 on day 14 (black arrow) after the inoculation. The fluorescence reading value after the stabilization was set as zero. The diurnal oscillations in O2 concentration reflect temperature changes induced by the proximity to the light bulb with a 12:12 h day:night cycle. Oxygen concentrations in all cultures were lower than 1 nM at all times after about 12 h and before the flushing on day 14. All data are representative of two independent measurements.

Extended Data Fig. 2 XRD spectra of biofilm samples incubated in the light for two weeks.

ad, These biofilms were not treated to remove manganese oxides before inoculation. a, One millimolar Mn(ii) and 0.05 mM Na2S. b, Mn(ii) at 0.1 mM, and 0.05 mM Na2S. c, One millimolar Mn(ii) and 1 mM Na2S. d, One millimolar Mn(ii) and 0.25 mM Na2S. Purple line shows the highest intensity peak at 2θ of 30.870° for the basal reflection of (104) plane of dolomite, CaMg(CO3)2. Red line shows the highest intensity peak at 2θ of 33.867° for the basal reflection of (121) plane of CaMnO3. Orange line shows the highest intensity peak at 2θ of 42.845° for the basal reflection of (110) plane of S0. All data are representative of three independent measurements.

Extended Data Fig. 3 XPS of the 2p spectral region of manganese in two-week-old microbial cultures.

a, Biofilm incubated in the dark. The Mn2p3/2 main peak of the sample fits the MnO standard at binding energy of 640.90 eV that corresponds to the redox state of Mn(ii). b, Biofilm incubated in the light. The Mn2p3/2 main peak of the sample fits the Mn3O4 standard at binding energy of 641.47 eV that corresponds to Mn(iii) and Mn(ii). c, Biofilm incubated in the light (a different region to that shown in b and d). The Mn2p3/2 main peak of the sample fits the Mn2O3 standard at binding energy of 641.61 eV that corresponds to Mn(iii). d, Biofilm incubated in the light (a different region to that shown in b, c). The Mn2p3/2 main peak of the sample fits MnO2 standard at binding energy of 641.90 eV that corresponds to redox state of Mn(iv). e, Biofilm incubated in the light (a different region to that shown in c, d). The Mn2p3/2 main peak of the sample fits the CaMnO3 standard at binding energy of 642.50 eV that corresponds to Mn(iv). All data are representative of three independent measurements.

Extended Data Fig. 4 Test of manganese-oxidizing activity in cell suspensions of photosynthetic cultures enriched under two conditions.

Results of XPS analysis of the 2p spectral region of manganese are shown. a, Culture enriched on 1 mM Mn(ii) and 0.05 mM H2S (condition (1)). The Mn2p3/2 main peak of the sample fits Mn3O4 standard at binding energy of 641.41 eV. This corresponds to Mn(ii) and Mn(iii). b, Culture enriched on 1 mM H2S (condition (2)). The Mn2p3/2 main peak of the sample fits MnO standard at binding energy of 640.97 eV and corresponds to the redox state Mn(ii).A detailed experimental protocol is described in ‘Interpretation of XPS spectra’ in the Methods, and summarized in Extended Data Table 3. All data are representative of three independent measurements.

Extended Data Fig. 5 Test of manganese-oxidizing activity in cell suspensions of pure cultures and co-cultures of C. limicola, C. tepidum and G. lovleyi.

ad, Results of XPS analysis of the 2p spectral region of manganese are shown. a, C. limicola, C. tepidum and G. lovleyi. The Mn2p3/2 main peak of the sample fits Mn2O3 standard at binding energy of 641.65 eV. This corresponds to a valence state of Mn(iii). b, C. limicola and C. tepidum. The Mn2p3/2 main peak of the sample fits MnCO3 standard at binding energy of 640.55 eV and corresponds to the redox state Mn(ii). c, C. limicola and G. lovleyi. The Mn2p3/2 main peak of the sample fits Mn3O4 standard at binding energy of 641.36eV. d, C. tepidum and G. lovleyi. The Mn2p3/2 main peak of the sample fits MnCO3 standard at binding energy of 640.57 eV. A detailed experimental protocol is described in ‘Probing the redox state of manganese in co-cultures’ in the Methods. All co-cultures were grown with 1 mM Mn(ii) and 0.05 mM H2S for 2 weeks in the light. All data are representative of three independent measurements.

Extended Data Fig. 6 Reticulate history of bacteriochlorophyll-biosynthesis genes supports a long history of phototrophy in the Chlorobiales stem lineage.

Horizontal gene transfers and gene duplications of bacteriochlorophyll genes were taken from a previous publication67. Age estimates for crown Chlorobi and GNS groups were taken from a previous publication26.

Extended Data Table 1 Aquatic environments with H2S and manganese in the photic zone
Extended Data Table 2 Shake tube and transfer procedures used to obtain enrichments from conditions 1 and 2
Extended Data Table 3 Summary of the methods used to examine the redox state of manganese in enrichment cultures
Extended Data Table 4 Mn(ii)-oxidation genes with confirmed function compared using BLASTp v. 2.6.0+ against the genome of C. limicola SR-12

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Daye, M., Klepac-Ceraj, V., Pajusalu, M. et al. Light-driven anaerobic microbial oxidation of manganese. Nature 576, 311–314 (2019). https://doi.org/10.1038/s41586-019-1804-0

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