Strong linkage between benthic oxygen uptake and bacterial tetraether lipids in deep-sea trench regions.

Oxygen in marine sediments regulates many key biogeochemical processes, playing a crucial role in shaping Earth's climate and benthic ecosystems. In this context, branched glycerol dialkyl glycerol tetraethers (brGDGTs), essential biomarkers in paleoenvironmental research, exhibit an as-yet-unresolved association with sediment oxygen conditions. Here, we investigated brGDGTs in sediments from three deep-sea regions (4045 to 10,100 m water depth) dominated by three respective trench systems and integrated the results with in situ oxygen microprofile data. Our results demonstrate robust correlations between diffusive oxygen uptake (DOU) obtained from microprofiles and brGDGT methylation and isomerization degrees, indicating their primary production within sediments and their strong linkage with microbial diagenetic activity. We establish a quantitative relationship between the Isomerization and Methylation index of Branched Tetraethers (IMBT) and DOU, suggesting its potential validity across deep-sea environments. Increased brGDGT methylation and isomerization likely enhance the fitness of source organisms in deep-sea habitats. Our study positions brGDGTs as a promising tool for quantifying benthic DOU in deep-sea settings, where DOU is a key metric for assessing sedimentary organic carbon degradation and microbial activity.

Dynamic redox and nutrient cycling response to climate forcing in the Mesoproterozoic ocean.

Controls on Mesoproterozoic ocean redox heterogeneity, and links to nutrient cycling and oxygenation feedbacks, remain poorly resolved. Here, we report ocean redox and phosphorus cycling across two high-resolution sections from the ~1.4 Ga Xiamaling Formation, North China Craton. In the lower section, fluctuations in trade wind intensity regulated the spatial extent of a ferruginous oxygen minimum zone, promoting phosphorus drawdown and persistent oligotrophic conditions. In the upper section, high but variable continental chemical weathering rates led to periodic fluctuations between highly and weakly euxinic conditions, promoting phosphorus recycling and persistent eutrophication. Biogeochemical modeling demonstrates how changes in geographical location relative to global atmospheric circulation cells could have driven these temporal changes in regional ocean biogeochemistry. Our approach suggests that much of the ocean redox heterogeneity apparent in the Mesoproterozoic record can be explained by climate forcing at individual locations, rather than specific events or step-changes in global oceanic redox conditions.

Respiration kinetics and allometric scaling in the demosponge Halichondria panicea.

BACKGROUND: The aquiferous system in sponges represents one of the simplest circulatory systems used by animals for the internal uptake and distribution of oxygen and metabolic substrates. Its modular organization enables sponges to metabolically scale with size differently than animals with an internal circulatory system. In this case, metabolic rate is typically limited by surface to volume constraints to maintain an efficient supply of oxygen and food. Here, we consider the linkeage between oxygen concentration, the respiration rates of sponges and sponge size. RESULTS: We explored respiration kinetics for individuals of the demosponge Halichondria panicea with varying numbers of aquiferous modules (nmodules = 1-102). From this work we establish relationships between the sponge size, module number, maximum respiration rate (Rmax) and the half-saturation constant, Km, which is the oxygen concentration producing half of the maximum respiration rate, Rmax. We found that the nmodules in H. panicea scales consistently with sponge volume (Vsp) and that Rmax increased with sponge size with a proportionality > 1. Conversly, we found a lack of correlation between Km and sponge body size suggesting that oxygen concentration does not control the size of sponges. CONCLUSIONS: The present study reveals that the addition of aquiferous modules (with a mean volume of 1.59 ± 0.22 mL) enables H. panicea in particular, and likely demosponges in general, to grow far beyond constraints limiting the size of their component modules and independent of ambient oxygen levels.

A case for an active eukaryotic marine biosphere during the Proterozoic era.

The microfossil record demonstrates the presence of eukaryotic organisms in the marine ecosystem by about 1,700 million years ago (Ma). Despite this, steranes, a biomarker indicator of eukaryotic organisms, do not appear in the rock record until about 780 Ma in what is known as the "rise of algae." Before this, it is argued that eukaryotes were minor ecosystem members, with prokaryotes dominating both primary production and ecosystem dynamics. In this view, the rise of algae was possibly sparked by increased nutrient availability supplying the higher nutrient requirements of eukaryotic algae. Here, we challenge this view. We use a size-based ecosystem model to show that the size distribution of preserved eukaryotic microfossils from 1,700 Ma and onward required an active eukaryote ecosystem complete with phototrophy, osmotrophy, phagotrophy, and mixotrophy. Model results suggest that eukaryotes accounted for one-half or more of the living biomass, with eukaryotic algae contributing to about one-half of total marine primary production. These ecosystems lived with deep-water phosphate levels of at least 10% of modern levels. The general lack of steranes in the pre-780-Ma rock record could be a result of poor preservation.

Microbe Profile: Nitrosopumilus maritimus.

Nitrosopumilus maritimus is a marine ammonia-oxidizing archaeon with a high affinity for ammonia. It fixes carbon via a modified hydroxypropionate/hydroxybutyrate cycle and shows weak utilization of cyanate as a supplementary energy and nitrogen source. When oxygen is depleted, N. maritimus produces its own oxygen, which may explain its regular occurrence in anoxic waters. Several enzymes of the ammonia oxidation and oxygen production pathways remain to be identified.

Metagenomic data for Halichondria panicea from Illumina and nanopore sequencing and preliminary genome assemblies for the sponge and two microbial symbionts.

OBJECTIVES: These data were collected to generate a novel reference metagenome for the sponge Halichondria panicea and its microbiome for subsequent differential expression analyses. DATA DESCRIPTION: These data include raw sequences from four separate sequencing runs of the metagenome of a single individual of Halichondria panicea-one Illumina MiSeq (2 × 300 bp, paired-end) run and three Oxford Nanopore Technologies (ONT) long-read sequencing runs, generating 53.8 and 7.42 Gbp respectively. Comparing assemblies of Illumina, ONT and an Illumina-ONT hybrid revealed the hybrid to be the 'best' assembly, comprising 163 Mbp in 63,555 scaffolds (N50: 3084). This assembly, however, was still highly fragmented and only contained 52% of core metazoan genes (with 77.9% partial genes), so it was also not complete. However, this sponge is an emerging model species for field and laboratory work, and there is considerable interest in genomic sequencing of this species. Although the resultant assemblies from the data presented here are suboptimal, this data note can inform future studies by providing an estimated genome size and coverage requirements for future sequencing, sharing additional data to potentially improve other suboptimal assemblies of this species, and outlining potential limitations and pitfalls of the combined Illumina and ONT approach to novel genome sequencing.

Oxygen and nitrogen production by an ammonia-oxidizing archaeon.

Ammonia-oxidizing archaea (AOA) are one of the most abundant groups of microbes in the world's oceans and are key players in the nitrogen cycle. Their energy metabolism­the oxidation of ammonia to nitrite­requires oxygen. Nevertheless, AOA are abundant in environments where oxygen is undetectable. By carrying out incubations for which oxygen concentrations were resolved to the nanomolar range, we show that after oxygen depletion, Nitrosopumilus maritimus produces dinitrogen and oxygen, which is used for ammonia oxidation. The pathway is not completely resolved but likely has nitric oxide and nitrous oxide as key intermediates. N. maritimus joins a handful of organisms known to produce oxygen in the dark. On the basis of this ability, we reevaluate the role of N. maritimus in oxygen-depleted marine environments.

A 200-million-year delay in permanent atmospheric oxygenation.

The rise of atmospheric oxygen fundamentally changed the chemistry of surficial environments and the nature of Earth's habitability1. Early atmospheric oxygenation occurred over a protracted period of extreme climatic instability marked by multiple global glaciations2,3, with the initial rise of oxygen concentration to above 10-5 of the present atmospheric level constrained to about 2.43 billion years ago4,5. Subsequent fluctuations in atmospheric oxygen levels have, however, been reported to have occurred until about 2.32 billion years ago4, which represents the estimated timing of irreversible oxygenation of the atmosphere6,7. Here we report a high-resolution reconstruction of atmospheric and local oceanic redox conditions across the final two glaciations of the early Palaeoproterozoic era, as documented by marine sediments from the Transvaal Supergroup, South Africa. Using multiple sulfur isotope and iron-sulfur-carbon systematics, we demonstrate continued oscillations in atmospheric oxygen levels after about 2.32 billion years ago that are linked to major perturbations in ocean redox chemistry and climate. Oxygen levels thus fluctuated across the threshold of 10-5 of the present atmospheric level for about 200 million years, with permanent atmospheric oxygenation finally arriving with the Lomagundi carbon isotope excursion at about 2.22 billion years ago, some 100 million years later than currently estimated.

Effects of Seasonal Anoxia on the Microbial Community Structure in Demosponges in a Marine Lake in Lough Hyne, Ireland.

Climate change is expanding marine oxygen minimum zones (OMZs), while anthropogenic nutrient input depletes oxygen concentrations locally. The effects of deoxygenation on animals are generally detrimental; however, some sponges (Porifera) exhibit hypoxic and anoxic tolerance through currently unknown mechanisms. Sponges harbor highly specific microbiomes, which can include microbes with anaerobic capabilities. Sponge-microbe symbioses must also have persisted through multiple anoxic/hypoxic periods throughout Earth's history. Since sponges lack key components of the hypoxia-inducible factor (HIF) pathway responsible for hypoxic responses in other animals, it was hypothesized that sponge tolerance to deoxygenation may be facilitated by its microbiome. To test this hypothesis, we determined the microbial composition of sponge species tolerating seasonal anoxia and hypoxia in situ in a semienclosed marine lake, using 16S rRNA amplicon sequencing. We discovered a high degree of cryptic diversity among sponge species tolerating seasonal deoxygenation, including at least nine encrusting species of the orders Axinellida and Poecilosclerida. Despite significant changes in microbial community structure in the water, sponge microbiomes were species specific and remarkably stable under varied oxygen conditions, which was further explored for Eurypon spp. 2 and Hymeraphia stellifera However, some symbiont sharing occurred under anoxia. At least three symbiont combinations, all including large populations of Thaumarchaeota, corresponded with deoxygenation tolerance, and some combinations were shared between some distantly related hosts. We propose hypothetical host-symbiont interactions following deoxygenation that could confer deoxygenation tolerance.IMPORTANCE The oceans have an uncertain future due to anthropogenic stressors and an uncertain past that is becoming clearer with advances in biogeochemistry. Both past and future oceans were, or will be, deoxygenated in comparison to present conditions. Studying how sponges and their associated microbes tolerate deoxygenation provides insights into future marine ecosystems. Moreover, sponges form the earliest branch of the animal evolutionary tree, and they likely resemble some of the first animals. We determined the effects of variable environmental oxygen concentrations on the microbial communities of several demosponge species during seasonal anoxia in the field. Our results indicate that anoxic tolerance in some sponges may depend on their symbionts, but anoxic tolerance was not universal in sponges. Therefore, some sponge species could likely outcompete benthic organisms like corals in future, reduced-oxygen ecosystems. Our results support the molecular evidence that sponges and other animals have a Neoproterozoic origin and that animal evolution was not limited by low-oxygen conditions.

The global explosion of eukaryotic algae: The potential role of phosphorus?

There arose one of the most important ecological transitions in Earth's history approximately 750 million years ago during the middle Neoproterozoic Era (1000 to 541 million years ago, Ma). Biomarker evidence suggests that around this time there was a rapid shift from a predominantly bacterial-dominated world to more complex ecosystems governed by eukaryotic primary productivity. The resulting 'Rise of the algae' led to dramatically altered food webs that were much more efficient in terms of nutrient and energy transfer. Yet, what triggered this ecological shift? In this study we examined the theory that it was the alleviation of phosphorus (P) deficiency that gave eukaryotic alga the prime opportunity to flourish. We performed laboratory experiments on the cyanobacterium Synechocystis salina and the eukaryotic algae Tetraselmis suecica and examined their ability to compete for phosphorus. Both these organisms co-occur in modern European coastal waters and are not known to have any allelopathic capabilities. The strains were cultured in mono and mixed cultures in chemostats across a range of dissolved inorganic phosphorus (DIP) concentrations to reflect modern and ancient oceanic conditions of 2 µM P and 0.2 µM P, respectively. Our results show that the cyanobacteria outcompete the algae at the low input (0.2 µM P) treatment, yet the eukaryotic algae were not completely excluded and remained a constant background component in the mixed-culture experiments. Also, despite their relatively large cell size, the algae T. suecica had a high affinity for DIP. With DIP input concentrations resembling modern-day levels (2 µM), the eukaryotic algae could effectively compete against the cyanobacteria in terms of total biomass production. These results suggest that the availability of phosphorus could have influenced the global expansion of eukaryotic algae. However, P limitation does not seem to explain the complete absence of eukaryotic algae in the biomarker record before ca. 750 Ma.

Very few sites can reshape the inferred phylogenetic tree.

The history of animal evolution, and the relative placement of extant animal phyla in this history is, in principle, testable from phylogenies derived from molecular sequence data. Though datasets have increased in size and quality in the past years, the contribution of individual genes (and ultimately amino acid sites) to the final phylogeny is unequal across genes. Here we demonstrate that removing a small fraction of sites strongly favoring one topology can produce a highly-supported tree of an alternate topology. We explore this approach using a dataset for animal phylogeny, and create a highly-supported tree with a monophyletic group of sponges and ctenophores, a topology not usually recovered. Because of the high sensitivity of such an analysis to gene selection, and because most gene sets are neither standardized nor representative of the entire genome, researchers should be diligent about making intermediate analyses available with their phylogenetic studies. Effort is needed to ensure these datasets are maximally informative, by ensuring all genes are systematically sampled across relevant species. From there, it could be determined whether any gene or gene sets introduce bias, and then deal with those biases appropriately.

Paleoenvironmental proxies and what the Xiamaling Formation tells us about the mid-Proterozoic ocean.

The Mesoproterozoic Era (1,600-1,000 million years ago, Ma) geochemical record is sparse, but, nevertheless, critical in untangling relationships between the evolution of eukaryotic ecosystems and the evolution of Earth-surface chemistry. The ca. 1,400 Ma Xiamaling Formation has experienced only very low-grade thermal maturity and has emerged as a promising geochemical archive informing on the interplay between climate, ecosystem organization, and the chemistry of the atmosphere and oceans. Indeed, the geochemical record of portions of the Xiamaling Formation has been used to place minimum constraints on concentrations of atmospheric oxygen as well as possible influences of climate and climate change on water chemistry and sedimentation dynamics. A recent study has argued, however, that some portions of the Xiamaling Formation deposited in a highly restricted environment with only limited value as a geochemical archive. In this contribution, we fully explore these arguments as well as the underlying assumptions surrounding the use of many proxies used for paleo-environmental reconstructions. In doing so, we pay particular attention to deep-water oxygen-minimum zone environments and show that these generate unique geochemical signals that have been underappreciated. These signals, however, are compatible with the geochemical record of those parts of the Xiamaling Formation interpreted as most restricted. Overall, we conclude that the Xiamaling Formation was most likely open to the global ocean throughout its depositional history. More broadly, we show that proper paleo-environmental reconstructions require an understanding of the biogeochemical signals generated in all relevant modern analogue depositional environments. We also evaluate new data on the δ98 Mo of Xiamaling Formation shales, revealing possible unknown pathways of molybdenum sequestration into sediments and concluding, finally, that seawater at that time likely had a δ98 Mo value of about 1.1‰.

Organism motility in an oxygenated shallow-marine environment 2.1 billion years ago.

Evidence for macroscopic life in the Paleoproterozoic Era comes from 1.8 billion-year-old (Ga) compression fossils [Han TM, Runnegar B (1992) Science 257:232-235; Knoll et al. (2006) Philos Trans R Soc Lond B 361:1023-1038], Stirling biota [Bengtson S et al. (2007) Paleobiology 33:351-381], and large colonial organisms exhibiting signs of coordinated growth from the 2.1-Ga Francevillian series, Gabon. Here we report on pyritized string-shaped structures from the Francevillian Basin. Combined microscopic, microtomographic, geochemical, and sedimentologic analyses provide evidence for biogenicity, and syngenicity and suggest that the structures underwent fossilization during early diagenesis close to the sediment-water interface. The string-shaped structures are up to 6 mm across and extend up to 170 mm through the strata. Morphological and 3D tomographic reconstructions suggest that the producer may have been a multicellular or syncytial organism able to migrate laterally and vertically to reach food resources. A possible modern analog is the aggregation of amoeboid cells into a migratory slug phase in cellular slime molds at times of starvation. This unique ecologic window established in an oxygenated, shallow-marine environment represents an exceptional record of the biosphere following the crucial changes that occurred in the atmosphere and ocean in the aftermath of the great oxidation event (GOE).

The Sirius Passet Lagerstätte of North Greenland-A geochemical window on early Cambrian low-oxygen environments and ecosystems.

The early Cambrian Sirius Passet fauna of northernmost Greenland (Cambrian Series 2, Stage 3) contains exceptionally preserved soft tissues that provide an important window to early animal evolution, while the surrounding sediment holds critical data on the palaeodepositional water-column chemistry. The present study combines palaeontological data with a multiproxy geochemical approach based on samples collected in situ at high stratigraphic resolution from Sirius Passet. After careful consideration of chemical alterations during burial, our results demonstrate that fossil preservation and biodiversity show significant correlation with iron enrichments (FeHR /FeT ), trace metal behaviour (V/Al), and changes in nitrogen cycling (δ15 N). These data, together with Mo/Al and the preservation of organic carbon (TOC), are consistent with a water column that was transiently low in oxygen concentration, or even intermittently anoxic. When compared with the biogeochemical characteristics of modern oxygen minimum zones (OMZs), geochemical and palaeontological data collectively suggest that oxygen concentrations as low as 0.2-0.4 ml/L restricted bioturbation but not the development of a largely nektobenthic community of predators and scavengers. We envisage for the Sirius Passet biota a depositional setting where anoxic water column conditions developed and passed over the depositional site, possibly in association with sea-level change, and where this early Cambrian biota was established in conditions with very low oxygen.

Rates and pathways of CH4 oxidation in ferruginous Lake Matano, Indonesia.

This study evaluates rates and pathways of methane (CH4 ) oxidation and uptake using 14 C-based tracer experiments throughout the oxic and anoxic waters of ferruginous Lake Matano. Methane oxidation rates in Lake Matano are moderate (0.36 nmol L-1  day-1 to 117 µmol L-1  day-1 ) compared to other lakes, but are sufficiently high to preclude strong CH4 fluxes to the atmosphere. In addition to aerobic CH4 oxidation, which takes place in Lake Matano's oxic mixolimnion, we also detected CH4 oxidation in Lake Matano's anoxic ferruginous waters. Here, CH4 oxidation proceeds in the apparent absence of oxygen (O2 ) and instead appears to be coupled to some as yet uncertain combination of nitrate ( NO 3 - ), nitrite ( NO 2 - ), iron (Fe) or manganese (Mn), or sulfate ( SO 4 2 - ) reduction. Throughout the lake, the fraction of CH4 carbon that is assimilated vs. oxidized to carbon dioxide (CO2 ) is high (up to 93%), indicating extensive CH4 conversion to biomass and underscoring the importance of CH4 as a carbon and energy source in Lake Matano and potentially other ferruginous or low productivity environments.

The aerobic diagenesis of Mesoproterozoic organic matter.

The Xiamaling Formation in the North China Block contains a well-preserved 1400 Ma sedimentary sequence with a low degree of thermal maturity. Previous studies have confirmed the dynamic and complex nature of this evolving marine setting, including the existence of an oxygen-minimum zone, using multi-proxy approaches, including iron speciation, trace metal dynamics, and organic geochemistry. Here, we investigate the prevailing redox conditions during diagenesis via the biomarkers of rearranged hopanes from the finely laminated sediments of the organic-rich black shales in Units 2 and 3 of the Xiamaling Formation. We find that rearranged hopanes are prominent in the biomarker composition of the oxygen-minimum zone sediment, which is completely different from that of the sediment in the overlying anoxic strata. Since the transition process from hopanes to rearranged hopanes requires oxygen via oxidation at the C-l6 alkyl position of 17α(H)-hopanes, we infer that dissolved oxygen led to the transformation of hopane precursors into rearranged hopanes during the early stages of diagenesis. The use of hopanoid hydrocarbons as biomarkers of marine redox conditions has rarely been previously reported, and the hydrocarbon signatures point towards oxic bottom waters during the deposition of Unit 3 of the Xiamaling Formation, which is consistent with the earlier oxygen-minimum zone environmental interpretation of this Unit.

Highly fractionated chromium isotopes in Mesoproterozoic-aged shales and atmospheric oxygen.

The history of atmospheric oxygen through the Mesoproterozoic Era is uncertain, but may have played a role in the timing of major evolutionary developments among eukaryotes. Previous work using chromium isotopes in sedimentary rocks has suggested that Mesoproterozoic Era atmospheric oxygen levels were too  low in concentration (<0.1% of present-day levels (PAL)) for the expansion of eukaryotic algae and for the evolution of crown-group animals that occurred later in the Neoproterozoic Era. In contrast, our new results on chromium isotopes from Mesoproterozoic-aged sedimentary rocks from the Shennongjia Group from South China is consistent with atmospheric oxygen concentrations of >1% PAL and thus the possibility that a permissive environment existed long before the expansion of various eukaryotic clades.

Decrypting the sulfur cycle in oceanic oxygen minimum zones.

Here we present ecophysiological studies of the anaerobic sulfide oxidizers considered critical to cryptic sulfur cycling in oceanic oxygen minimum zones (OMZs). We find that HS- oxidation rates by microorganisms in the Chilean OMZ offshore from Dichato are sufficiently rapid (18 nM h-1), even at HS- concentrations well below 100 nM, to oxidize all sulfide produced during sulfate reduction in OMZs. Even at 100 nM, HS- is well below published half-saturation concentrations and we conclude that the sulfide-oxidizing bacteria in OMZs (likely the SUP05/ARTIC96BD lineage of the gammaproteobacteria) have high-affinity (>105 g-1 wet cells h-1) sulfur uptake systems. These specific affinities for sulfide are higher than those recorded for any other organism on any other substrate. Such high affinities likely allow anaerobic sulfide oxidizers to maintain vanishingly low sulfide concentrations in OMZs driving marine cryptic sulfur cycling. If more broadly distributed, such high-affinity sulfur biochemistry could facilitate sulfide-based metabolisms and prominent S-cycles in many other ostensibly sulfide-free environments.

A Mesoproterozoic iron formation.

We describe a 1,400 million-year old (Ma) iron formation (IF) from the Xiamaling Formation of the North China Craton. We estimate this IF to have contained at least 520 gigatons of authigenic Fe, comparable in size to many IFs of the Paleoproterozoic Era (2,500-1,600 Ma). Therefore, substantial IFs formed in the time window between 1,800 and 800 Ma, where they are generally believed to have been absent. The Xiamaling IF is of exceptionally low thermal maturity, allowing the preservation of organic biomarkers and an unprecedented view of iron-cycle dynamics during IF emplacement. We identify tetramethyl aryl isoprenoid (TMAI) biomarkers linked to anoxygenic photosynthetic bacteria and thus phototrophic Fe oxidation. Although we cannot rule out other pathways of Fe oxidation, iron and organic matter likely deposited to the sediment in a ratio similar to that expected for anoxygenic photosynthesis. Fe reduction was likely a dominant and efficient pathway of organic matter mineralization, as indicated by organic matter maturation by Rock Eval pyrolysis combined with carbon isotope analyses: Indeed, Fe reduction was seemingly as efficient as oxic respiration. Overall, this Mesoproterozoic-aged IF shows many similarities to Archean-aged (>2,500 Ma) banded IFs (BIFs), but with an exceptional state of preservation, allowing an unprecedented exploration of Fe-cycle dynamics in IF deposition.