The nature of the last universal common ancestor and its impact on the early Earth system.

The nature of the last universal common ancestor (LUCA), its age and its impact on the Earth system have been the subject of vigorous debate across diverse disciplines, often based on disparate data and methods. Age estimates for LUCA are usually based on the fossil record, varying with every reinterpretation. The nature of LUCA's metabolism has proven equally contentious, with some attributing all core metabolisms to LUCA, whereas others reconstruct a simpler life form dependent on geochemistry. Here we infer that LUCA lived ~4.2 Ga (4.09-4.33 Ga) through divergence time analysis of pre-LUCA gene duplicates, calibrated using microbial fossils and isotope records under a new cross-bracing implementation. Phylogenetic reconciliation suggests that LUCA had a genome of at least 2.5 Mb (2.49-2.99 Mb), encoding around 2,600 proteins, comparable to modern prokaryotes. Our results suggest LUCA was a prokaryote-grade anaerobic acetogen that possessed an early immune system. Although LUCA is sometimes perceived as living in isolation, we infer LUCA to have been part of an established ecological system. The metabolism of LUCA would have provided a niche for other microbial community members and hydrogen recycling by atmospheric photochemistry could have supported a modestly productive early ecosystem.

Eukaryogenesis and oxygen in Earth history.

The endosymbiotic origin of mitochondria during eukaryogenesis has long been viewed as an adaptive response to the oxygenation of Earth's surface environment, presuming a fundamentally aerobic lifestyle for the free-living bacterial ancestors of mitochondria. This oxygen-centric view has been robustly challenged by recent advances in the Earth and life sciences. While the permanent oxygenation of the atmosphere above trace concentrations is now thought to have occurred 2.2 billion years ago, large parts of the deep ocean remained anoxic until less than 0.5 billion years ago. Neither fossils nor molecular clocks correlate the origin of mitochondria, or eukaryogenesis more broadly, to either of these planetary redox transitions. Instead, mitochondria-bearing eukaryotes are consistently dated to between these two oxygenation events, during an interval of pervasive deep-sea anoxia and variable surface-water oxygenation. The discovery and cultivation of the Asgard archaea has reinforced metabolic evidence that eukaryogenesis was initially mediated by syntrophic H2 exchange between an archaeal host and an α-proteobacterial symbiont living under anoxia. Together, these results temporally, spatially and metabolically decouple the earliest stages of eukaryogenesis from the oxygen content of the surface ocean and atmosphere. Rather than reflecting the ancestral metabolic state, obligate aerobiosis in eukaryotes is most probably derived, having only become globally widespread over the past 1 billion years as atmospheric oxygen approached modern levels.

Selection for Gaia across Multiple Scales.

Recently postulated mechanisms and models can help explain the enduring 'Gaia' puzzle of environmental regulation mediated by life. Natural selection can produce nutrient recycling at local scales and regulation of heterogeneous environmental variables at ecosystem scales. However, global-scale environmental regulation involves a temporal and spatial decoupling of effects from actors that makes conventional evolutionary explanations problematic. Instead, global regulation can emerge by a process of 'sequential selection' in which systems that destabilize their environment are short-lived and result in extinctions and reorganizations until a stable attractor is found. Such persistence-enhancing properties can in turn increase the likelihood of acquiring further persistence-enhancing properties through 'selection by survival alone'. Thus, Earth system feedbacks provide a filter for persistent combinations of macroevolutionary innovations.

The effects of marine eukaryote evolution on phosphorus, carbon and oxygen cycling across the Proterozoic-Phanerozoic transition.

A 'Neoproterozoic oxygenation event' is widely invoked as a causal factor in animal evolution, and often attributed to abiotic causes such as post-glacial pulses of phosphorus weathering. However, recent evidence suggests a series of transient ocean oxygenation events ∼660-520 Ma, which do not fit the simple model of a monotonic rise in atmospheric oxygen (pO2). Hence, we consider mechanisms by which the evolution of marine eukaryotes, coupled with biogeochemical and ecological feedbacks, potentially between alternate stable states, could have caused changes in ocean carbon cycling and redox state, phosphorus cycling and atmospheric pO2. We argue that the late Tonian ocean ∼750 Ma was dominated by rapid microbial cycling of dissolved organic matter (DOM) with elevated nutrient (P) levels due to inefficient removal of organic matter to sediments. We suggest the abrupt onset of the eukaryotic algal biomarker record ∼660-640 Ma was linked to an escalation of protozoan predation, which created a 'biological pump' of sinking particulate organic matter (POM). The resultant transfer of organic carbon (Corg) and phosphorus to sediments was strengthened by subsequent eukaryotic innovations, including the advent of sessile benthic animals and mobile burrowing animals. Thus, each phase of eukaryote evolution tended to lower P levels and oxygenate the ocean on ∼104 year timescales, but by decreasing Corg/P burial ratios, tended to lower atmospheric pO2 and deoxygenate the ocean again on ∼106 year timescales. This can help explain the transient nature and ∼106 year duration of oceanic oxygenation events through the Cryogenian-Ediacaran-Cambrian.

Atmospheric oxygen regulation at low Proterozoic levels by incomplete oxidative weathering of sedimentary organic carbon.

It is unclear why atmospheric oxygen remained trapped at low levels for more than 1.5 billion years following the Paleoproterozoic Great Oxidation Event. Here, we use models for erosion, weathering and biogeochemical cycling to show that this can be explained by the tectonic recycling of previously accumulated sedimentary organic carbon, combined with the oxygen sensitivity of oxidative weathering. Our results indicate a strong negative feedback regime when atmospheric oxygen concentration is of order pO2∼0.1 PAL (present atmospheric level), but that stability is lost at pO2<0.01 PAL. Within these limits, the carbonate carbon isotope (δ13C) record becomes insensitive to changes in organic carbon burial rate, due to counterbalancing changes in the weathering of isotopically light organic carbon. This can explain the lack of secular trend in the Precambrian δ13C record, and reopens the possibility that increased biological productivity and resultant organic carbon burial drove the Great Oxidation Event.

Biogeochemical Transformations in the History of the Ocean.

The ocean has undergone several profound biogeochemical transformations in its 4-billion-year history, and these were an integral part of the coevolution of life and the planet. This review focuses on changes in ocean redox state as controlled by changes in biological activity, nutrient concentrations, and atmospheric O2. Motivated by disparate interpretations of available geochemical data, we aim to show how quantitative modeling-spanning microbial mats, shelf seas, and the open ocean-can help constrain past ocean biogeochemical redox states and show what caused transformations between them. We outline key controls on ocean redox structure and review pertinent proxies and their interpretation. We then apply this quantitative framework to three key questions: How did the origin of oxygenic photosynthesis transform ocean biogeochemistry? How did the Great Oxidation transform ocean biogeochemistry? And how was ocean biogeochemistry transformed in the Neoproterozoic-Paleozoic?

Matworld - the biogeochemical effects of early life on land.

Contents 531 I. 531 II. 532 III. 534 IV. 535 V. 535 VI. 535 Acknowledgements 536 References 536 SUMMARY: There is growing evidence that life has been on land for billions of years. Microbial mats fuelled by oxygenic photosynthesis were probably present in terrestrial habitats from c. 3.0 billion yr ago (Ga) onwards, creating localized 'oxygen oases' under a reducing atmosphere, which left a characteristic oxidative weathering signal. After the Great Oxidation c. 2.4 Ga, the now oxidizing atmosphere masked that redox signal, but ancient soils record the mobilization of phosphorus and other elements by organic acids in weathering profiles. Evidence for Neoproterozoic 'greening of the land' and intensification of weathering c. 0.85-0.54 Ga is currently equivocal. However, the mid-Palaeozoic c. 0.45-0.4 Ga shows global atmospheric changes consistent with increased terrestrial productivity and intensified weathering by the first land plants.

Earliest land plants created modern levels of atmospheric oxygen.

The progressive oxygenation of the Earth's atmosphere was pivotal to the evolution of life, but the puzzle of when and how atmospheric oxygen (O2) first approached modern levels (∼21%) remains unresolved. Redox proxy data indicate the deep oceans were oxygenated during 435-392 Ma, and the appearance of fossil charcoal indicates O2 >15-17% by 420-400 Ma. However, existing models have failed to predict oxygenation at this time. Here we show that the earliest plants, which colonized the land surface from ∼470 Ma onward, were responsible for this mid-Paleozoic oxygenation event, through greatly increasing global organic carbon burial-the net long-term source of O2 We use a trait-based ecophysiological model to predict that cryptogamic vegetation cover could have achieved ∼30% of today's global terrestrial net primary productivity by ∼445 Ma. Data from modern bryophytes suggests this plentiful early plant material had a much higher molar C:P ratio (∼2,000) than marine biomass (∼100), such that a given weathering flux of phosphorus could support more organic carbon burial. Furthermore, recent experiments suggest that early plants selectively increased the flux of phosphorus (relative to alkalinity) weathered from rocks. Combining these effects in a model of long-term biogeochemical cycling, we reproduce a sustained +2‰ increase in the carbonate carbon isotope (δ(13)C) record by ∼445 Ma, and predict a corresponding rise in O2 to present levels by 420-400 Ma, consistent with geochemical data. This oxygen rise represents a permanent shift in regulatory regime to one where fire-mediated negative feedbacks stabilize high O2 levels.

Bridging the gap between omics and earth system science to better understand how environmental change impacts marine microbes.

The advent of genomic-, transcriptomic- and proteomic-based approaches has revolutionized our ability to describe marine microbial communities, including biogeography, metabolic potential and diversity, mechanisms of adaptation, and phylogeny and evolutionary history. New interdisciplinary approaches are needed to move from this descriptive level to improved quantitative, process-level understanding of the roles of marine microbes in biogeochemical cycles and of the impact of environmental change on the marine microbial ecosystem. Linking studies at levels from the genome to the organism, to ecological strategies and organism and ecosystem response, requires new modelling approaches. Key to this will be a fundamental shift in modelling scale that represents micro-organisms from the level of their macromolecular components. This will enable contact with omics data sets and allow acclimation and adaptive response at the phenotype level (i.e. traits) to be simulated as a combination of fitness maximization and evolutionary constraints. This way forward will build on ecological approaches that identify key organism traits and systems biology approaches that integrate traditional physiological measurements with new insights from omics. It will rely on developing an improved understanding of ecophysiology to understand quantitatively environmental controls on microbial growth strategies. It will also incorporate results from experimental evolution studies in the representation of adaptation. The resulting ecosystem-level models can then evaluate our level of understanding of controls on ecosystem structure and function, highlight major gaps in understanding and help prioritize areas for future research programs. Ultimately, this grand synthesis should improve predictive capability of the ecosystem response to multiple environmental drivers.

Multiple environmental controls on phytoplankton growth strategies determine adaptive responses of the N : P ratio.

The controls on the 'Redfield' N : P stoichiometry of marine phytoplankton and hence the N : P ratio of the deep ocean remain incompletely understood. Here, we use a model for phytoplankton ecophysiology and growth, based on functional traits and resource-allocation trade-offs, to show how environmental filtering, biotic interactions, and element cycling in a global ecosystem model determine phytoplankton biogeography, growth strategies and macromolecular composition. Emergent growth strategies capture major observed patterns in marine biomes. Using a new synthesis of experimental RNA and protein measurements to constrain per-ribosome translation rates, we determine a spatially variable lower limit on adaptive rRNA:protein allocation and hence on the relationship between the largest cellular P and N pools. Comparison with the lowest observed phytoplankton N : P ratios and N : P export fluxes in the Southern Ocean suggests that additional contributions from phospholipid and phosphorus storage compounds play a fundamental role in determining the marine biogeochemical cycling of these elements.