Stony corals exhibit striking morphological plasticity across diverse environments and trophic strategies, raising fundamental questions about the conservation of their biomineralization machinery. Here, we characterize the skeletal organic matrix (SOM) proteome of the cosmopolitan cold-water, asymbiotic coral Desmophyllum pertusum and compare it with published skeletal proteomes from a facultatively photosymbiotic temperate coral and an obligately photosymbiotic subtropical coral. Despite pronounced differences in habitat, symbiotic status, and skeletal micro-density, we observe convergence on a conserved biomineralization toolkit spanning these taxa. Comparative proteomics, genomics, and AI-based structural predictions reveal that this toolkit integrates acidic matrix proteins, carbonic anhydrases, adhesion and structural proteins, and signaling components with multiple export pathways, including secretion, vesicle-mediated trafficking, and cytoskeleton-associated transport. The current proteome expands the diversity of acidic proteins, suggesting roles not only in stabilizing amorphous calcium carbonate but also in proton buffering within intracellular and extracellular calcifying compartments. Together, these findings redefine coral biomineralization as a dynamic, coordinated network of cellular pathways rather than a static assemblage of matrix components. By establishing D. pertusum as a symbiont-free model system, this work provides a mechanistic framework for dissecting coral calcification across environments and for assessing the resilience of this conserved machinery to ongoing ocean change.

Life is far from thermodynamic equilibrium. Hence, life must extract energy from the environment. On Earth, that energy is driven by networks of metabolic reactions in all cells which ultimately move electrons and protons (i.e. hydrogen atoms) across the planet. The origin of metabolism required the emergence and evolution of proteins. Proteins are nanometre-scale chemical machines-i.e. literal nanomachines which physically move. These nanomachines enable living systems to perform essential biochemical tasks from replication to metabolism; the latter being the engines of life. In all extant life on Earth, a small set of these nanomachines, called oxidoreductases, couple chemical energy from the environment with core redox reactions including photosynthesis, respiration and nitrogen fixation. The origins and emergence of complex life have been intimately tied with evolution of oxidoreductases. Here, using structure-based analyses, we describe the evolution of the protein catalysts in three biological epochs. First, thermodynamically driven polymerization reactions generated simple metal-binding peptides with specific sequences that catalysed core metabolic reactions. Second, these catalysts were incorporated in small structural 'folds'. In the third epoch, these folds served as building blocks for extant, complex nanomachines.This article is part of the discussion meeting issue 'Chance and purpose in the evolution of biospheres'.

Nitrogen and phosphorus are the two macro-nutrients that limit biological productivity in the ocean. While the supply of P depends on geological processes, N is biologically supplied from an inexhaustible atmospheric source, but can be limited by micro-nutrients, especially iron. Here we present a record of N and C isotopes over the past 165 Ma in marine sediments to address feedbacks between the N-cycle and productivity. Over most of the last 165 Myr, the fixed N averaged +3.2‰, (-2 and +9‰), but higher in distal areas of the ocean due to limited vertical mixing. Using an isotope box model and a coupled climate model we show that this is caused by winds that induce upwelling changing due to continental meander. Upwelling along low latitude east-west orientated Tethyan coastlines results in low δ15N, while upwelling along narrow N-S coastlines as it does today, results in high δ15N due to denitrification.

Oxygenic photosynthesis requires excitation energy transfer from light-harvesting complexes (LHCs) to reaction centers (RCs) to drive photochemical redox chemistry. The effective absorption cross section of RCs dynamically responds to the light environment on time scales of seconds to days, allowing rapid acclimations to changes in spectral irradiance and photoprotection under high light, thereby optimizing light absorption for photochemistry. Although energy coupling between LHC-RCs has been studied for decades in laboratory cultures, it remains poorly understood in real-world conditions, where it is potentially influenced by nutrients. In the oceans, one of the most critical micronutrients for photosynthesis is iron (Fe). To investigate the effects of Fe stress on the energetic coupling between LHC-RCs in natural phytoplankton assemblages in the Southern Atlantic Ocean, we assessed photophysiological responses using a pair of custom-built fluorometers measuring chlorophyll-a variable fluorescence and picosecond fluorescence lifetimes. Detailed analysis based on the functional absorption cross section of the oxygen-evolving complex, quantum yield of photochemistry, energetic connectivity of RCs, and the average lifetime of in vivo chlorophyll fluorescence suggested that between 10 and 25% of LHCs remain uncoupled from RCs and do not effectively contribute to photochemical charge separation. Addition of Fe to samples under trace metal-clean on-board incubations indicates relatively rapid recoupling (< 24 h) of antennae to photochemistry, followed by biophysical stabilization of recoupled complexes. Our findings highlight the crucial role of micronutrients in controlling the excitation energy transfer from LHCs to RCs in marine phytoplankton and the overall primary productivity in the real-world oceans.

Abstract Nitrogen and phosphorus are the two macro-nutrients that limit biological productivity in the ocean. N is supplied by the biological fixation of N2 from a virtually inexhaustible atmospheric source whereas the supply of P depends on geological processes. However, N2 fixation can be limited by micro-nutrients, especially iron. To address the feedbacks between the N-cycle and productivity on geological timescales, we present a record of N and C isotopes over the past 165 Ma in marine sediments. The N isotope composition of the deep ocean averages 3.2‰, and while relatively stable for most of this time, did range between -2 and +9‰. In comparison, exported production in distal areas of the ocean over the last 90 Myr averages 7.0‰, and ranges between +3 and +11‰, with the greatest difference from deepwater occurring when vertical mixing was limited. These significant multi-million-year time scale fluctuations result from interactions between plate tectonics and ocean biogeochemistry. We further present a coupled climate model that shows that winds that induce upwelling change due to continental meander. Importantly, the response of N cycling to changes in upwelling differs as those centers have moved in response to continent configuration. Upwelling induced productivity along low latitude east-west orientated Tethyan coastlines was elevated throughout much of the late Jurassic to Eocene. As Tethys closed, changing N dynamics are recorded by high δ15N, arising from increased N losses from the water column compared to burial in sediments. As upwelling increased again in the late Miocene, albeit weaker than before, along north-south coasts with narrow shelves, and ocean fronts became more pronounced, another abrupt increase in δ15N occurred. The implications on N-fixation is that meridional overturning circulation has separated areas of N-fixation and upwelling, leading to limitation by N in the modern ocean, unlike the situation of Tethys. However, limitation of N-fixation by Fe in the vast Panthalassic Ocean led to the most severe N-starvation.

Foraminifera are unicellular protists capable of precipitating calcite tests, which fossilize and preserve geochemical signatures of past environmental conditions dating back to the Cambrian period. The biomineralization mechanisms responsible for the mineral structures, which are key to interpreting palaeoceanographic signals, are poorly understood. Here, we present an extensive analysis of the test-bound proteins. Using liquid chromatography-tandem mass spectrometry, we identify 373 test-bound proteins in the large benthic foraminifer Amphistegina lobifera, the majority of which are highly acidic and rich in negatively charged residues. We detect proteins involved in vesicle formation and active Ca2+ trafficking, but in contrast, do not find similar proteins involved in Mg2+ transport. Considering findings from this study and previous ones, we propose a dual ion transport model involving seawater vacuolization, followed by the active release of Ca2+ from the initial vacuoles and subsequent uptake into newly formed Ca-rich vesicles that consequently enrich the calcification fluid. We further speculate that Mg2+ passively leaks through the membrane from the remaining Mg-rich vesicles, into the calcifying fluid, at much lower concentrations than in seawater. This hypothesis could not only explain the low Mg/Ca ratio in foraminiferal tests compared to inorganic calcite, but could possibly also account for its elevated sensitivity to temperature compared with inorganically precipitated CaCO3.

Phytoplankton in the ocean account for less than 1% of the global photosynthetic biomass, but contribute about 45% of the photosynthetically fixed carbon on Earth. This amazing production/biomass ratio implies a very high photosynthetic efficiency. But, how efficiently is the absorbed light used in marine photosynthesis? The introduction of picosecond and then femtosecond lasers for kinetic measurements in mid 1970s to 90 s was a revolution in basic photosynthesis research that vastly improved our understanding of the energy conversion processes in photosynthetic reactions. Until recently, the use of this technology in the ocean was not feasible due to the complexity of related instrumentation and the lack of picosecond lasers suitable for routine operation in the field. However, recent advances in solid-state laser technology and the development of compact data acquisition electronics led to the application of picosecond fluorescence lifetime analyses in the field. Here, we review the development of operational ultrasensitive picosecond fluorescence instruments to infer photosynthetic energy conversion processes in ocean ecosystems. This analysis revealed that, in spite of the high production/biomass ratio in marine phytoplankton, the photosynthetic energy conversion efficiency is exceptionally low—on average, ca. 50% of its maximum potential, suggesting that most of the contemporary open ocean surface waters are extremely nutrient deficient.

Of the six elements incorporated into the major polymers of life, phosphorus is the least abundant on a global scale [E. Anders, M. Ebihara, Geochim. Cosmochim. Acta 46, 2363-2380 (1982)] and has been described as the "ultimate limiting nutrient" [T. Tyrrell, Nature 400, 525-531 (1999)]. In the modern ocean, the supply of dissolved phosphorus is predominantly sustained by the oxidative remineralization/recycling of organic phosphorus in seawater. However, in the Archean Eon (4 to 2.5 Ga), surface waters were anoxic and reducing. Here, we conducted photochemical experiments to test whether photodegradation of ubiquitous dissolved organic phosphorus could facilitate phosphorus recycling under the simulated Archean conditions. Our results strongly suggest that organic phosphorus compounds, which were produced by marine biota (e.g., adenosine monophosphate and phosphatidylserine) or delivered by meteorites (e.g., methyl phosphonate) can undergo rapid photodegradation and release inorganic phosphate into solution under anoxic conditions. Our experimental results and theoretical calculations indicate that photodegradation of organic phosphorus could have been a significant source of bioavailable phosphorus in the early ocean and would have fueled primary production during the Archean eon.

Unlike most higher plants, unicellular algae can acclimate to changes in irradiance on time scales of hours to a few days. The process involves an enigmatic signaling pathway originating in the plastid that leads to coordinated changes in plastid and nuclear gene expression. To deepen our understanding of this process, we conducted functional studies to examine how the model diatom, Phaeodactylum tricornutum, acclimates to low light and sought to identify the molecules responsible for the phenomenon. We show that two transformants with altered expression of two putative signal transduction molecules, a light-specific soluble kinase and a plastid transmembrane protein, that appears to be regulated by a long noncoding natural antisense transcript, arising from the opposite strand, are physiologically incapable of photoacclimation. Based on these results, we propose a working model of the retrograde feedback in the signaling and regulation of photoacclimation in a marine diatom.

Ancestral metabolic processes involve the reversible oxidation of molecular hydrogen by hydrogenase. Extant hydrogenase enzymes are complex, comprising hundreds of amino acids and multiple cofactors. We designed a 13–amino acid nickel-binding peptide capable of robustly producing molecular hydrogen from protons under a wide variety of conditions. The peptide forms a di-nickel cluster structurally analogous to a Ni-Fe cluster in [NiFe] hydrogenase and the Ni-Ni cluster in acetyl-CoA synthase, two ancient, extant proteins central to metabolism. These experimental results demonstrate that modern enzymes, despite their enormous complexity, likely evolved from simple peptide precursors on early Earth.

The core metabolic reactions of life drive electrons through a class of redox protein enzymes, the oxidoreductases. The energetics of electron flow is determined by the redox potentials of organic and inorganic cofactors as tuned by the protein environment. Understanding how protein structure affects oxidation-reduction energetics is crucial for studying metabolism, creating bioelectronic systems, and tracing the history of biological energy utilization on Earth. We constructed ProtReDox (https://protein-redox-potential.web.app), a manually curated database of experimentally determined redox potentials. With over 500 measurements, we can begin to identify how proteins modulate oxidation-reduction energetics across the tree of life. By mapping redox potentials onto networks of oxidoreductase fold evolution, we can infer the evolution of electron transfer energetics over deep time. ProtReDox is designed to include user-contributed submissions with the intention of making it a valuable resource for researchers in this field.

The redox state of the plastoquinone (PQ) pool is a known sensor for retrograde signaling. In this paper, we asked, "does the redox state of the PQ pool modulate the saturation state of thylakoid lipids?" Data from fatty acid composition and mRNA transcript abundance analyses suggest a strong connection between these two aspects in a model marine diatom. Fatty acid profiles of Phaeodactylum tricornutum exhibited specific changes when the redox state of the PQ pool was modulated by light and two chemical inhibitors [3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) or 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone (DBMIB)]. Data from liquid chromatography with tandem mass spectrometry (LC-MS/MS) indicated a ca. 7-20% decrease in the saturation state of all four conserved thylakoid lipids in response to an oxidized PQ pool. The redox signals generated from an oxidized PQ pool in plastids also increased the mRNA transcript abundance of nuclear-encoded C16 fatty acid desaturases (FADs), with peak upregulation on a timescale of 6 to 12 h. The connection between the redox state of the PQ pool and thylakoid lipid saturation suggests a heretofore unrecognized retrograde signaling pathway that couples photosynthetic electron transport and the physical state of thylakoid membrane lipids.

In the Equatorial Atlantic nitrogen availability is assumed to control phytoplankton dynamics. However, in situ measurements of phytoplankton physiology and productivity are surprisingly sparse in comparison with the North Atlantic. In addition to the formation of the Equatorial cold tongue in the boreal summer, tropical instability waves (TIWs) and related short-term processes may locally cause episodic events of enhanced nutrient supply to the euphotic layer. Here, we assess changes in phytoplankton photophysiology in response to such episodic events as well as short-term nutrient addition experiments using a pair of custom-built fluorometers that measure chlorophyll a (Chl a) variable fluorescence and fluorescence lifetimes. The fluorometers were deployed during a transatlantic cruise along the Equator in the fall of 2019. We hypothesized that the Equatorial Atlantic is nitrogen-limited, with an increasing degree of limitation to the west where the cold tongue is not prominent, and that infrequent nitrate injection by TIW related processes are the primary source alleviating this limitation. We further hypothesized phytoplankton are well acclimated to the low levels of nitrogen, and once nitrogen is supplied, they can rapidly utilize it to stimulate growth and productivity. Across three TIW events encountered, we observed increased productivity and chlorophyll a concentration concurrent with a decreased photochemical conversion efficiency and overall photophysiological competency. Moreover, the observed decrease in photosynthetic turnover rates toward the western section suggested a 70% decrease in growth rates compared to their maximum values under nutrient-replete conditions. This decrease aligned with the increased growth rates observed following 24 h incubation with added nitrate in the western section. These results support our hypotheses that nitrogen is the limiting factor in the region and that phytoplankton are in a state of balanced growth, waiting to “body surf” waves of nutrients which fuel growth and productivity.

Protein coordinated iron-sulfur clusters drive electron flow within metabolic pathways for organisms throughout the tree of life. It is not known how iron-sulfur clusters were first incorporated into proteins. Structural analogies to iron-sulfide minerals present on early Earth, suggest a connection in the evolution of both proteins and minerals. The availability of large protein and mineral crystallographic structure data sets, provides an opportunity to explore co-evolution of proteins and minerals on a large-scale using informatics approaches. However, quantitative comparisons are confounded by the infinite, repeating nature of the mineral lattice, in contrast to metal clusters in proteins, which are finite in size. We address this problem using the Niggli reduction to transform a mineral lattice to a finite, unique structure that when translated reproduces the crystal lattice. Protein and reduced mineral structures were represented as quotient graphs with the edges and nodes corresponding to bonds and atoms, respectively. We developed a graph theory-based method to calculate the maximum common connected edge subgraph (MCCES) between mineral and protein quotient graphs. MCCES can accommodate differences in structural volumes and easily allows additional chemical criteria to be considered when calculating similarity. To account for graph size differences, we use the Tversky similarity index. Using consistent criteria, we found little similarity between putative ancient iron-sulfur protein clusters and iron-sulfur mineral lattices, suggesting these metal sites are not as evolutionarily connected as once thought. We discuss possible evolutionary implications of these findings in addition to suggesting an alternative proxy, mineral surfaces, for better understanding the coevolution of the geosphere and biosphere.

Contextualized correspondence traces the emergence of a provocative hypothesis.

Sulfur is an essential element of life that is assimilated by Earth's biosphere through the chemical breakdown of pyrite. On the early Earth, pyrite weathering by atmospheric oxygen was severely limited, and low marine sulfate concentrations persisted for much of the Archean eon. Here, we show an anoxic photochemical mechanism of pyrite weathering that could have provided substantial amounts of sulfate to the oceans as continents formed in the late Archean. Pyrite grains suspended in anoxic ferrous iron solutions produced millimolar sulfate concentrations when irradiated with ultraviolet light. The Fe2+(aq) was photooxidized, which, in turn, led to the chemical oxidation of pyritic sulfur. Additional experiments conducted with 2.68 Ga shale demonstrated that photochemically derived ferric iron oxidizes and dissolves sedimentary pyrite during chemical weathering. The results suggest that before the rise of atmospheric oxygen, oxidative pyrite weathering on Archean continents was controlled by the exposure of land to sunlight.