Jena E. Johnson

Manganese-oxidizing photosynthesis before the rise of cyanobacteria

The emergence of oxygen-producing (oxygenic) photosynthesis fundamentally transformed our planet; however, the processes that led to the evolution of biological water splitting have remained largely unknown. To illuminate this history, we examined the behavior of the ancient Mn cycle using newly obtained scientific drill cores through an early Paleoproterozoic succession (2.415 Ga) preserved in South Africa. These strata contain substantial Mn enrichments (up to ∼17 wt %) well before those associated with the rise of oxygen such as the ∼2.2 Ga Kalahari Mn deposit. Using microscale X-ray spectroscopic techniques coupled to optical and electron microscopy and carbon isotope ratios, we demonstrate that the Mn is hosted exclusively in carbonate mineral phases derived from reduction of Mn oxides during diagenesis of primary sediments. Additional observations of independent proxies for O2—multiple S isotopes (measured by isotope-ratio mass spectrometry and secondary ion mass spectrometry) and redox-sensitive detrital grains—reveal that the original Mn-oxide phases were not produced by reactions with O2, which points to a different high-potential oxidant. These results show that the oxidative branch of the Mn cycle predates the rise of oxygen, and provide strong support for the hypothesis that the water-oxidizing complex of photosystem II evolved from a former transitional photosystem capable of single-electron oxidation reactions of Mn.

O2 constraints from Paleoproterozoic detrital pyrite and uraninite

Redox-sensitive detrital grains such as pyrite and uraninite in sedimentary successions provide one of the most conspicuous geological clues to a different composition of the Archean and early Paleoproterozoic atmosphere. Today, these minerals are rapidly chemically weathered within short transport distances. Prior to the rise of oxygen, low O2 concentrations allowed their survival in siliciclastic deposits with grain erosion tied only to physical transport processes. After the rise of oxygen, redox-sensitive detrital grains effectively vanish from the sedimentary record. To get a better understanding of the timing of this transition, we examined sandstones recorded in a scientifi c drill core from the South African 2.415 Ga Koegas Subgroup, a mixed siliciclastic and iron formation–bearing unit deposited on the western deltaic margin of the Kaapvaal craton in early Paleoproterozoic time. We observed detrital pyrite and uraninite grains throughout all investigated sandstone beds in the section, indicating the rise of oxygen is younger than 2.415 Ga. To better understand how observations of detrital pyrite and uraninite in sedimentary rocks can quantitatively constrain Earth surface redox conditions, we constructed a model of grain erosion from chemical weathering and physical abrasion to place an upper limit on ancient environmental O2 concentrations. Even conservative model calculations for deltaic depositional systems with suffi cient transport distances (approximately hundreds of kilometers) show that redox-sensitive detrital grains are remarkably sensitive to environmental O2 concentrations, and they constrain the Archean and early Paleoproterozoic atmosphere to have <3.2 × 10 –5 atm of molecular O2. These levels are lower than previously hypothesized for redox-sensitive detrital grains, but they are consistent with estimates made from other redox proxy data, including the anomalous fractionation of sulfur isotopes. The binary loss of detrital pyrite and uraninite from the sedimentary record coincident with the rise of oxygen indicates that atmospheric O2 concentrations rose substantially at this time and were never again suffi ciently low (<0.01 atm) to enable survival and preservation of these grains in short transport systems.

SQUID-SIMS is a useful approach to uncover primary signals in the Archean sulfur cycle

Significance A challenge to understanding ancient sulfur-cycle processes on early Earth is the persistent observation that postdepositional processes have affected all Archean-age rocks, impacting geochemical signals, and the quality of paleoenvironmental interpretations. To solve this problem we developed a combination of texture-specific microscale techniques—scanning high-resolution low-temperature superconducting quantum interference device microscopy and secondary ion mass spectrometry. We applied these techniques in a well-studied Archean-age sedimentary succession in South Africa to unravel the mineralization and isotopic history and reveal primary sulfur-cycle processes. We observed systematic patterns of isotope ratios at microscopic scales that inform the nature of enigmatic sulfur-isotope mass anomalies unique to this time interval and further support hypotheses for the early evolution of sulfate-reduction metabolisms. Many aspects of Earth’s early sulfur cycle, from the origin of mass-anomalous fractionations to the degree of biological participation, remain poorly understood—in part due to complications from postdepositional diagenetic and metamorphic processes. Using a combination of scanning high-resolution magnetic superconducting quantum interference device (SQUID) microscopy and secondary ion mass spectrometry (SIMS) of sulfur isotopes (32S, 33S, and 34S), we examined drill core samples from slope and basinal environments adjacent to a major Late Archean (∼2.6–2.5 Ga) marine carbonate platform from South Africa. Coupled with petrography, these techniques can untangle the complex history of mineralization in samples containing diverse sulfur-bearing phases. We focused on pyrite nodules, precipitated in shallow sediments. These textures record systematic spatial differences in both mass-dependent and mass-anomalous sulfur-isotopic composition over length scales of even a few hundred microns. Petrography and magnetic imaging demonstrate that mass-anomalous fractionations were acquired before burial and compaction, but also show evidence of postdepositional alteration 500 million y after deposition. Using magnetic imaging to screen for primary phases, we observed large spatial gradients in Δ33S (>4‰) in nodules, pointing to substantial environmental heterogeneity and dynamic mixing of sulfur pools on geologically rapid timescales. In other nodules, large systematic radial δ34S gradients (>20‰) were observed, from low values near their centers increasing to high values near their rims. These fractionations support hypotheses that microbial sulfate reduction was an important metabolism in organic-rich Archean environments—even in an Archean ocean basin dominated by iron chemistry.

Manganese and the Evolution of Photosynthesis

Oxygenic photosynthesis is the most important bioenergetic event in the history of our planet—it evolved once within the Cyanobacteria, and remained largely unchanged as it was transferred to algae and plants via endosymbiosis. Manganese plays a fundamental role in this history because it lends the critical redox behavior of the water-oxidizing complex of photosystem II. Constraints from the photoassembly of the Mn-bearing water-oxidizing complex fuel the hypothesis that Mn(II) once played a key role as an electron donor for anoxygenic photosynthesis prior to the evolution of oxygenic photosynthesis. Here we review the growing body of geological and geochemical evidence from the Archean and Paleoproterozoic sedimentary records that supports this idea and demonstrates that the oxidative branch of the Mn cycle switched on prior to the rise of oxygen. This Mn-oxidizing phototrophy hypothesis also receives support from the biological record of extant phototrophs, and can be made more explicit by leveraging constraints from structural biology and biochemistry of photosystem II in Cyanobacteria. These observations highlight that water-splitting in photosystem II evolved independently from a homodimeric ancestral type II reaction center capable of high potential photosynthesis and Mn(II) oxidation, which is required by the presence of homologous redox-active tyrosines in the modern heterodimer. The ancestral homodimer reaction center also evolved a C-terminal extension that sterically precluded standard phototrophic electron donors like cytochrome c, cupredoxins, or high-potential iron-sulfur proteins, and could only complete direct oxidation of small molecules like Mn2+, and ultimately water.

Real-Time Manganese Phase Dynamics during Biological and Abiotic Manganese Oxide Reduction

Manganese oxides are often highly reactive and easily reduced, both abiotically, by a variety of inorganic chemical species, and biologically during anaerobic respiration by microbes. To evaluate the reaction mechanisms of these different reduction routes and their potential lasting products, we measured the sequence progression of microbial manganese(IV) oxide reduction mediated by chemical species (sulfide and ferrous iron) and the common metal-reducing microbe Shewanella oneidensis MR-1 under several endmember conditions, using synchrotron X-ray spectroscopic measurements complemented by X-ray diffraction and Raman spectroscopy on precipitates collected throughout the reaction. Crystalline or potentially long-lived phases produced in these experiments included manganese(II)-phosphate, manganese(II)-carbonate, and manganese(III)-oxyhydroxides. Major controls on the formation of these discrete phases were alkalinity production and solution conditions such as inorganic carbon and phosphate availability. The formation of a long-lived Mn(III) oxide appears to depend on aqueous Mn(2+) production and the relative proportion of electron donors and electron acceptors in the system. These real-time measurements identify mineralogical products during Mn(IV) oxide reduction, contribute to understanding the mechanism of various Mn(IV) oxide reduction pathways, and assist in interpreting the processes occurring actively in manganese-rich environments and recorded in the geologic record of manganese-rich strata.

Reply to Jones and Crowe: Correcting mistaken views of sedimentary geology, Mn-oxidation rates, and molecular clocks

Jones and Crowe (1) raise issues already addressed in our article (2) based on an inaccurate grasp of the literature and several logical misconceptions. The authors suggest that inputs we chose in our kinetic calculations are unsuitable because we used values only from the Black Sea. As described, we made an extremely conservative estimate because the Black Sea is the most rapid Mn-oxidizing environment in the literature. Other locations have oxidation rates orders-of-magnitude lower (3). Jones and Crowe also propose sedimentation rates in our Mn-oxidation calculations were too high, citing a reference for incorrect rocks: different lithologies, environments, process sedimentology, geodynamic setting, and age. The paper they cite estimated long-term rates for the 2642–2521 Ma Campbellrand Subgroup, deposited >100 million y earlier on a marine platform rather than Koegas continental margin deltaic sediments. Using correct sedimentary geology is important (2).

Genomics of a phototrophic nitrite oxidizer: insights into the evolution of photosynthesis and nitrification

Oxygenic photosynthesis evolved from anoxygenic ancestors before the rise of oxygen ~2.32 billion years ago; however, little is known about this transition. A high redox potential reaction center is a prerequisite for the evolution of the water-oxidizing complex of photosystem II. Therefore, it is likely that high-potential phototrophy originally evolved to oxidize alternative electron donors that utilized simpler redox chemistry, such as nitrite or Mn. To determine whether nitrite could have had a role in the transition to high-potential phototrophy, we sequenced and analyzed the genome of Thiocapsa KS1, a Gammaproteobacteria capable of anoxygenic phototrophic nitrite oxidation. The genome revealed a high metabolic flexibility, which likely allows Thiocapsa KS1 to colonize a great variety of habitats and to persist under fluctuating environmental conditions. We demonstrate that Thiocapsa KS1 does not utilize a high-potential reaction center for phototrophic nitrite oxidation, which suggests that this type of phototrophic nitrite oxidation did not drive the evolution of high-potential phototrophy. In addition, phylogenetic and biochemical analyses of the nitrite oxidoreductase (NXR) from Thiocapsa KS1 illuminate a complex evolutionary history of nitrite oxidation. Our results indicate that the NXR in Thiocapsa originates from a different nitrate reductase clade than the NXRs in chemolithotrophic nitrite oxidizers, suggesting that multiple evolutionary trajectories led to modern nitrite-oxidizing bacteria.