Direct evidence for eoarchean iron metabolism?

Metasedimentary rocks from Isua, West Greenland (> 3,700 million years old) contain carbonaceous compounds, compatible with a biogenic origin (Hassenkam, Andersson, Dalby, Mackenzie, & Rosing, 2017; Ohtomo, Kakegawa, Ishida, Nagase, & Rosing, 2014; Rosing, 1999). The metamorphic mineral assemblage with garnet and quartz intergrowths contains layers of carbonaceous inclusions contiguous with carbon-rich sedimentary beds in the host rock. Previous studies (Hassenkam et al., 2017; Ohtomo et al., 2014; Rosing, 1999) on Isua rocks focused on testing the biogenic origin of the carbonaceous material, but here we searched for evidence which could provide new insights into the nature of the life that generated this carbonaceous material. We studied material trapped in inclusions armoured within quartz grains inside garnet porphyroblasts by non-destructive ptychographic X-ray nanotomography (PXCT). The 3D electron density maps generated by PXCT were correlated with maps from X-ray fluorescence tomography and micro-Raman spectroscopy. We found that the material trapped inside inclusions in the quartz grains consist of disordered carbon material encasing domains of iron-rich carbonaceous material. These results corroborate earlier claims (Hassenkam et al., 2017; Ohtomo et al., 2014; Rosing, 1999) for biogenic origins and are compatible with relics of metamorphosed biological material originally containing high iron/carbon ratios, comparable to ratios found in most extant organisms. These iron-rich domains represent the oldest evidence for organic iron complexes in the geologic record and are consistent with Fe-isotopic evidence for metabolic iron fractionation in > 3,700 Ma Isua banded iron formation (Czaja et al., 2013; Whitehouse & Fedo, 2007).

Building mountain biodiversity: Geological and evolutionary processes.

Mountain regions are unusually biodiverse, with rich aggregations of small-ranged species that form centers of endemism. Mountains play an array of roles for Earth's biodiversity and affect neighboring lowlands through biotic interchange, changes in regional climate, and nutrient runoff. The high biodiversity of certain mountains reflects the interplay of multiple evolutionary mechanisms: enhanced speciation rates with distinct opportunities for coexistence and persistence of lineages, shaped by long-term climatic changes interacting with topographically dynamic landscapes. High diversity in most tropical mountains is tightly linked to bedrock geology-notably, areas comprising mafic and ultramafic lithologies, rock types rich in magnesium and poor in phosphate that present special requirements for plant physiology. Mountain biodiversity bears the signature of deep-time evolutionary and ecological processes, a history well worth preserving.

Author Correction: Reassessing evidence of life in 3,700-million-year-old rocks of Greenland.

In Extended Data Fig. 1 of this Letter, the map showed the field-work location incorrectly; this figure has been corrected online.

Reassessing evidence of life in 3,700-million-year-old rocks of Greenland.

The Palaeoarchean supracrustal belts in Greenland contain Earth's oldest rocks and are a prime target in the search for the earliest evidence of life on Earth. However, metamorphism has largely obliterated original rock textures and compositions, posing a challenge to the preservation of biological signatures. A recent study of 3,700-million-year-old rocks of the Isua supracrustal belt in Greenland described a rare zone in which low deformation and a closed metamorphic system allowed preservation of primary sedimentary features, including putative conical and domical stromatolites1 (laminated accretionary structures formed by microbially mediated sedimentation). The morphology, layering, mineralogy, chemistry and geological context of the structures were attributed to the formation of microbial mats in a shallow marine environment by 3,700 million years ago, at the start of Earth's rock record. Here we report new research that shows a non-biological, post-depositional origin for the structures. Three-dimensional analysis of the morphology and orientation of the structures within the context of host rock fabrics, combined with texture-specific analyses of major and trace element chemistry, show that the 'stromatolites' are more plausibly interpreted as part of an assemblage of deformation structures formed in carbonate-altered metasediments long after burial. The investigation of the structures of the Isua supracrustal belt serves as a cautionary tale in the search for signs of past life on Mars, highlighting the importance of three-dimensional, integrated analysis of morphology, rock fabrics and geochemistry at appropriate scales.

Bacterial natural transformation by highly fragmented and damaged DNA.

DNA molecules are continuously released through decomposition of organic matter and are ubiquitous in most environments. Such DNA becomes fragmented and damaged (often <100 bp) and may persist in the environment for more than half a million years. Fragmented DNA is recognized as nutrient source for microbes, but not as potential substrate for bacterial evolution. Here, we show that fragmented DNA molecules (≥ 20 bp) that additionally may contain abasic sites, cross-links, or miscoding lesions are acquired by the environmental bacterium Acinetobacter baylyi through natural transformation. With uptake of DNA from a 43,000-y-old woolly mammoth bone, we further demonstrate that such natural transformation events include ancient DNA molecules. We find that the DNA recombination is RecA recombinase independent and is directly linked to DNA replication. We show that the adjacent nucleotide variations generated by uptake of short DNA fragments escape mismatch repair. Moreover, double-nucleotide polymorphisms appear more common among genomes of transformable than nontransformable bacteria. Our findings reveal that short and damaged, including truly ancient, DNA molecules, which are present in large quantities in the environment, can be acquired by bacteria through natural transformation. Our findings open for the possibility that natural genetic exchange can occur with DNA up to several hundreds of thousands years old.

The elusive Hadean enriched reservoir revealed by 142Nd deficits in Isua Archaean rocks.

The first indisputable evidence for very early differentiation of the silicate Earth came from the extinct (146)Sm-(142)Nd chronometer. (142)Nd excesses measured in 3.7-billion-year (Gyr)-old rocks from Isua (southwest Greenland) relative to modern terrestrial samples imply their derivation from a depleted mantle formed in the Hadean eon (about 4,570-4,000 Gyr ago). As dictated by mass balance, the differentiation event responsible for the formation of the Isua early-depleted reservoir must also have formed a complementary enriched component. However, considerable efforts to find early-enriched mantle components in Isua have so far been unsuccessful. Here we show that the signature of the Hadean enriched reservoir, complementary to the depleted reservoir in Isua, is recorded in 3.4-Gyr-old mafic dykes intruding into the Early Archaean rocks. Five out of seven dykes carry (142)Nd deficits compared to the terrestrial Nd standard, with three samples yielding resolvable deficits down to -10.6 parts per million. The enriched component that we report here could have been a mantle reservoir that differentiated owing to the crystallization of a magma ocean, or could represent a mafic proto-crust that separated from the mantle more than 4.47 Gyr ago. Our results testify to the existence of an enriched component in the Hadean, and may suggest that the southwest Greenland mantle preserved early-formed heterogeneities until at least 3.4 Gyr ago.

Isotope composition and volume of Earth's early oceans.

Oxygen and hydrogen isotope compositions of Earth's seawater are controlled by volatile fluxes among mantle, lithospheric (oceanic and continental crust), and atmospheric reservoirs. Throughout geologic time the oxygen mass budget was likely conserved within these Earth system reservoirs, but hydrogen's was not, as it can escape to space. Isotopic properties of serpentine from the approximately 3.8 Ga Isua Supracrustal Belt in West Greenland are used to characterize hydrogen and oxygen isotope compositions of ancient seawater. Archaean oceans were depleted in deuterium [expressed as δD relative to Vienna standard mean ocean water (VSMOW)] by at most 25 ± 5‰, but oxygen isotope ratios were comparable to modern oceans. Mass balance of the global hydrogen budget constrains the contribution of continental growth and planetary hydrogen loss to the secular evolution of hydrogen isotope ratios in Earth's oceans. Our calculations predict that the oceans of early Earth were up to 26% more voluminous, and atmospheric CH(4) and CO(2) concentrations determined from limits on hydrogen escape to space are consistent with clement conditions on Archaean Earth.

Early Archean serpentine mud volcanoes at Isua, Greenland, as a niche for early life.

The Isua Supracrustal Belt, Greenland, of Early Archean age (3.81-3.70 Ga) represents the oldest crustal segment on Earth. Its complex lithology comprises an ophiolite-like unit and volcanic rocks reminiscent of boninites, which tie Isua supracrustals to an island arc environment. We here present zinc (Zn) isotope compositions measured on serpentinites and other rocks from the Isua supracrustal sequence and on serpentinites from modern ophiolites, midocean ridges, and the Mariana forearc. In stark contrast to modern midocean ridge and ophiolite serpentinites, Zn in Isua and Mariana serpentinites is markedly depleted in heavy isotopes with respect to the igneous average. Based on recent results of Zn isotope fractionation between coexisting species in solution, the Isua serpentinites were permeated by carbonate-rich, high-pH hydrothermal solutions at medium temperature (100-300 °C). Zinc isotopes therefore stand out as a pH meter for fossil hydrothermal solutions. The geochemical features of the Isua fluids resemble the interstitial fluids sampled in the mud volcano serpentinites of the Mariana forearc. The reduced character and the high pH inferred for these fluids make Archean serpentine mud volcanoes a particularly favorable setting for the early stabilization of amino acids.

Coupled 182W-142Nd constraint for early Earth differentiation.

Recent high precision (142)Nd isotope measurements showed that global silicate differentiation may have occurred as early as 30-75 Myr after the Solar System formation [Bennett V, et al. (2007) Science 318:1907-1910]. This time scale is almost contemporaneous with Earth's core formation at approximately 30 Myr [Yin Q, et al. (2002) Nature 418:949-952]. The (182)Hf-(182)W system provides a powerful complement to the (142)Nd results for early silicate differentiation, because both core formation and silicate differentiation fractionate Hf from W. Here we show that eleven terrestrial samples from diverse tectonic settings, including five early Archean samples from Isua, Greenland, of which three have been previously shown with (142)Nd anomalies, all have a homogeneous W isotopic composition, which is approximately 2epsilon-unit more radiogenic than the chondritic value. By using a 3-stage model calculation that describes the isotopic evolution in chondritic reservoir and core segregation, as well as silicate differentiation, we show that the W isotopic composition of terrestrial samples provides the most stringent time constraint for early core formation (27.5-38 Myr) followed by early terrestrial silicate differentiation (38-75 Myr) that is consistent with the terrestrial (142)Nd anomalies.

No climate paradox under the faint early Sun.

Environmental niches in which life first emerged and later evolved on the Earth have undergone dramatic changes in response to evolving tectonic/geochemical cycles and to biologic interventions, as well as increases in the Sun's luminosity of about 25 to 30 per cent over the Earth's history. It has been inferred that the greenhouse effect of atmospheric CO(2) and/or CH(4) compensated for the lower solar luminosity and dictated an Archaean climate in which liquid water was stable in the hydrosphere. Here we demonstrate, however, that the mineralogy of Archaean sediments, particularly the ubiquitous presence of mixed-valence Fe(II-III) oxides (magnetite) in banded iron formations is inconsistent with such high concentrations of greenhouse gases and the metabolic constraints of extant methanogens. Prompted by this, and the absence of geologic evidence for very high greenhouse-gas concentrations, we hypothesize that a lower albedo on the Earth, owing to considerably less continental area and to the lack of biologically induced cloud condensation nuclei, made an important contribution to moderating surface temperature in the Archaean eon. Our model calculations suggest that the lower albedo of the early Earth provided environmental conditions above the freezing point of water, thus alleviating the need for extreme greenhouse-gas concentrations to satisfy the faint early Sun paradox.

Early anaerobic metabolisms.

Before the advent of oxygenic photosynthesis, the biosphere was driven by anaerobic metabolisms. We catalogue and quantify the source strengths of the most probable electron donors and electron acceptors that would have been available to fuel early-Earth ecosystems. The most active ecosystems were probably driven by the cycling of H2 and Fe2+ through primary production conducted by anoxygenic phototrophs. Interesting and dynamic ecosystems would have also been driven by the microbial cycling of sulphur and nitrogen species, but their activity levels were probably not so great. Despite the diversity of potential early ecosystems, rates of primary production in the early-Earth anaerobic biosphere were probably well below those rates observed in the marine environment. We shift our attention to the Earth environment at 3.8Gyr ago, where the earliest marine sediments are preserved. We calculate, consistent with the carbon isotope record and other considerations of the carbon cycle, that marine rates of primary production at this time were probably an order of magnitude (or more) less than today. We conclude that the flux of reduced species to the Earth surface at this time may have been sufficient to drive anaerobic ecosystems of sufficient activity to be consistent with the carbon isotope record. Conversely, an ecosystem based on oxygenic photosynthesis was also possible with complete removal of the oxygen by reaction with reduced species from the mantle.