Balance and imbalance in biogeochemical cycles reflect the operation of closed, exchange, and open sets.

Biogeochemical reactions modulate the chemical composition of the oceans and atmosphere, providing feedbacks that sustain planetary habitability over geological time. Here, we mathematically evaluate a suite of biogeochemical processes to identify combinations of reactions that stabilize atmospheric carbon dioxide by balancing fluxes of chemical species among the ocean, atmosphere, and geosphere. Unlike prior modeling efforts, this approach does not prescribe functional relationships between the rates of biogeochemical processes and environmental conditions. Our agnostic framework generates three types of stable reaction combinations: closed sets, where sources and sinks mutually cancel for all chemical reservoirs; exchange sets, where constant ocean-atmosphere conditions are maintained through the growth or destruction of crustal reservoirs; and open sets, where balance in alkalinity and carbon fluxes is accommodated by changes in other chemical components of seawater or the atmosphere. These three modes of operation have different characteristic timescales and may leave distinct evidence in the rock record. To provide a practical example of this theoretical framework, we applied the model to recast existing hypotheses for Cenozoic climate change based on feedbacks or shared forcing mechanisms. Overall, this work provides a systematic and simplified conceptual framework for understanding the function and evolution of global biogeochemical cycles.

Erratum: Publisher Correction: Enhanced clay formation key in sustaining the Middle Eocene Climatic Optimum.

[This corrects the article DOI: 10.1038/s41561-023-01234-y.].

Enhanced clay formation key in sustaining the Middle Eocene Climatic Optimum.

The Middle Eocene Climatic Optimum (around 40 million years ago) was a roughly 400,000-year-long global warming phase associated with an increase in atmospheric CO2 concentrations and deep-ocean acidification that interrupted the Eocene's long-term cooling trend. The unusually long duration, compared with early Eocene global warming phases, is puzzling as temperature-dependent silicate weathering should have provided a negative feedback, drawing down CO2 over this timescale. Here we investigate silicate weathering during this climate warming event by measuring lithium isotope ratios (reported as δ7Li), which are a tracer for silicate weathering processes, from a suite of open-ocean carbonate-rich sediments. We find a positive δ7Li excursion-the only one identified for a warming event so far -of ~3‰. Box model simulations support this signal to reflect a global shift from congruent weathering, with secondary mineral dissolution, to incongruent weathering, with secondary mineral formation. We surmise that, before the climatic optimum, there was considerable soil shielding of the continents. An increase in continental volcanism initiated the warming event, but it was sustained by an increase in clay formation, which sequestered carbonate-forming cations, short-circuiting the carbonate-silicate cycle. Clay mineral dynamics may play an important role in the carbon cycle for climatic events occurring over intermediate (i.e., 100,000 year) timeframes.

Quantification of 68 elements in river water monitoring samples in single-run measurements.

Triple-quadrupole inductively coupled plasma mass spectrometry (ICP-QQQ-MS) is a unique analytical technique which is, next to speciation analyses, applied for the determination of total element concentrations in several matrices. Due to its wide linear range, short analysis times, and the collision-reaction gas technology, it is capable of addressing a high number of analytes in a single run with sufficient low limits of quantification for river water monitoring. Over the last decades, the focus of the environmental monitoring changed from "traditional" and regulated analytes to elements of possibly rising concern from new applications such as the so-called technology-critical elements (TCE). By widening the analytical window of this method for applications in networks of future river water monitoring, a better understanding of natural transport processes and global biogeochemical element cycles will be established and the total number of methods can be reduced. During method development and validation, certified reference materials, calibration check solutions, and spiked river water samples from 12 major German rivers covering different catchment areas were measured and evaluated with the three cell gases He, H2 and O2. The method delivers a best as possible undisturbed simultaneous determination for 68 out of 71 target analytes with recoveries in an accepted range of 80-120% for river water samples (dissolved fraction; <0.45 µm). After comprehensive evaluation, we offer a novel best-practice multi-element method for river water monitoring with the goal of fostering the exchange and discussion between practitioners in long-term river monitoring. It enables the readers to create their own methods based on the scientific needs to monitor elemental "fingerprints" of rivers and their catchments.

Weak environmental adaptation of rare phylotypes sustaining soil multi-element cycles in response to decades-long fertilization.

Deciphering the ecological role of soil communities in the maintenance of multiple ecosystem functions is pivotal for the conservation and sustainability of soil biodiversity. However, few studies have investigated niche differentiation of abundant and rare microbiota, as well as their contributions to multiple soil elemental cycles, particularly in agroecosystems that have received decades of intense fertilization. Here, we characterized the environmental thresholds and phylogenetic signals for the environmental adaptation of both abundant and rare microbial subcommunities via amplicon sequencing and metagenomic sequencing and explored their importance in sustaining soil multiple nutrient cycling in agricultural fields that were fertilized for two decades. The results showed that rare taxa exhibited narrower niche breadths and weaker phylogenetic signals than abundant species. The assembly of abundant subcommunity was shaped predominantly by dispersal limitation (explained 71.1 % of the variation in bacteria) and undominated processes (explained 75 % of the variation in fungi), whereas the assembly of rare subcommunity was dominated by homogeneous selection process (explained 100 % of the variation in bacteria and 60 % of the variation in fungi). Soil ammonia nitrogen was the leading factor mediating the balance between stochastic and deterministic processes in both abundant (R2 = 0.15, P < 0.001) and rare (R2 = 0.08, P < 0.001) bacterial communities. Notably, the rare biosphere largely contributed to key soil processes such as carbon (R2bacteria = 0.03, P < 0.05; R2fungi = 0.05, P < 0.05) and nitrogen (R2bacteria = 0.03, P < 0.05; R2fungi = 0.17, P < 0.001) cycling. Collectively, these findings facilitate our understanding of the maintenance of rhizosphere bacterial and fungal diversity in response to agricultural fertilization and highlight the key role of rare taxa in sustaining agricultural ecosystem functions.

Routes to reduction of phosphate by high-energy events.

Phosphate minerals such as those in the apatite group tend to be the dominant forms of phosphorus in minerals on the Earth's surface. Phosphate can be reduced to phosphides during high-energy events, such as lightning and impacts. Here we show that, in addition to formation of metal phosphides, a new compound was formed by lightning in a fulgurite from New Port Richey, Florida, USA. A calcium phosphite material, ideally CaHPO3, was found in spherules mainly consisting of iron silicides that formed by lightning-induced fusion of sand around a tree root. This phosphite material bears a phosphorus oxidation state intermediate of that of phosphides and phosphates in a geologic sample and implicates phosphites as being potentially relevant to other high-energy events where phosphorus may partially change its redox state, and material similar to this phosphite may also be the source of phosphite that makes up part of the phosphorus biogeochemical cycle.

Viruses of sulfur oxidizing phototrophs encode genes for pigment, carbon, and sulfur metabolisms.

Viral infections modulate bacterial metabolism and ecology. Here, we investigated the hypothesis that viruses influence the ecology of purple and green sulfur bacteria in anoxic and sulfidic lakes, analogs of euxinic oceans in the geologic past. By screening metagenomes from lake sediments and water column, in addition to publicly-available genomes of cultured purple and green sulfur bacteria, we identified almost 300 high and medium-quality viral genomes. Viruses carrying the gene psbA, encoding the small subunit of photosystem II protein D1, were ubiquitous, suggesting viral interference with the light reactions of sulfur oxidizing autotrophs. Viruses predicted to infect these autotrophs also encoded auxiliary metabolic genes for reductive sulfur assimilation as cysteine, pigment production, and carbon fixation. These observations show that viruses have the genomic potential to modulate the production of metabolic markers of phototrophic sulfur bacteria that are used to identify photic zone euxinia in the geologic past.

Global patterns in marine organic matter stoichiometry driven by phytoplankton ecophysiology.

The proportion of major elements in marine organic matter links cellular processes to global nutrient, oxygen and carbon cycles. Differences in the C:N:P ratios of organic matter have been observed between ocean biomes, but these patterns have yet to be quantified from the underlying small-scale physiological and ecological processes. Here we use an ecosystem model that includes adaptive resource allocation within and between ecologically distinct plankton size classes to attribute the causes of global patterns in the C:N:P ratios. We find that patterns of N:C variation are largely driven by common physiological adjustment strategies across all phytoplankton, while patterns of N:P are driven by ecological selection for taxonomic groups with different phosphorus storage capacities. Although N:C varies widely due to cellular adjustment to light and nutrients, its latitudinal gradient is modest because of depth-dependent trade-offs between nutrient and light availability. Strong latitudinal variation in N:P reflects an ecological balance favouring small plankton with lower P storage capacity in the subtropics, and larger eukaryotes with a higher cellular P storage capacity in nutrient-rich high latitudes. A weaker N:P difference between southern and northern hemispheres, and between the Atlantic and Pacific oceans, reflects differences in phosphate available for cellular storage. Despite simulating only two phytoplankton size classes, the emergent global variability of elemental ratios resembles that of all measured species, suggesting that the range of growth conditions and ecological selection sustain the observed diversity of stoichiometry among phytoplankton.

Global patterns and predictors of C:N:P in marine ecosystems.

Oceanic nutrient cycles are coupled, yet carbon-nitrogen-phosphorus (C:N:P) stoichiometry in marine ecosystems is variable through space and time, with no clear consensus on the controls on variability. Here, we analyze hydrographic, plankton genomic diversity, and particulate organic matter data from 1970 stations sampled during a global ocean observation program (Bio-GO-SHIP) to investigate the biogeography of surface ocean particulate organic matter stoichiometry. We find latitudinal variability in C:N:P stoichiometry, with surface temperature and macronutrient availability as strong predictors of stoichiometry at high latitudes. Genomic observations indicated community nutrient stress and suggested that nutrient supply rate and nitrogen-versus-phosphorus stress are predictive of hemispheric and regional variations in stoichiometry. Our data-derived statistical model suggests that C:P and N:P ratios will increase at high latitudes in the future, however, changes at low latitudes are uncertain. Our findings suggest systematic regulation of elemental stoichiometry among ocean ecosystems, but that future changes remain highly uncertain.

Stable ocean redox during the main phase of the Great Ordovician Biodiversification Event.

The Great Ordovician Biodiversification Event (GOBE) represents the greatest increase in marine animal biodiversity ever recorded. What caused this transformation is heavily debated. One hypothesis states that rising atmospheric oxygen levels drove the biodiversification based on the premise that animals require oxygen for their metabolism. Here, we present uranium isotope data from a Middle Ordovician marine carbonate succession that shows the steepest rise in generic richness occurred with global marine redox stability. Ocean oxygenation ensued later and could not have driven the biodiversification. Stable marine anoxic zones prevailed during the maximum increase in biodiversity (Dapingian-early Darriwilian) when the life expectancy of evolving genera greatly increased. Subsequently, unstable ocean redox conditions occurred together with a marine carbon cycle disturbance and a decrease in relative diversification rates. Therefore, we propose that oceanic redox stability was a factor in facilitating the establishment of more resilient ecosystems allowing marine animal life to radiate.

Dissolved trace element concentrations and fluxes in the Irrawaddy, Salween, Sittaung and Kaladan Rivers.

The Irrawaddy (Ayeyarwaddy) and Salween (Thanlwin) globally rank among the largest rivers for supplying dissolved and particulate material to the ocean. Along with the Sittaung and Kaladan rivers they have societal importance to Myanmar in terms water sources and food production. Despite their importance for global biogeochemical cycles and the ~50 million people who live in their catchments, the chemistry of these rivers is poorly known. This study presents a comprehensive survey of dissolved (<0.22 µm) trace element concentrations (Sr, Fe, Al, Ba, Mn, V, Rb, Cu, Zn, As, Li, Ni, Mo, Cr, U, Pb, Sb, Co, Cs, Tl and Cd) at 38 locations within these river catchments, spanning a period of 2 years. The results highlight the global importance of the Irrawaddy and Salween rivers for trace element global biogeochemical cycles; contributing between 1 and 17 % of global dissolved riverine fluxes to the land-ocean interface for the studied elements. Area normalized dissolved fluxes in these catchments are ~2 to 10 times higher than global average values for most elements, consistent with high rates of chemical weathering. In general, anthropogenic activities have yet to significantly perturb dissolved trace element fluxes in these river systems. The presented dataset should therefore serve as a useful 'natural' baseline, against which future perturbations driven by climate change and/or the development of Myanmar's mining industry could be assessed. Exceptions to this include As in the Sittaung River and Sb, Zn, Pb and As in the Salween River, which may already be significantly impacted by anthropogenic inputs. The former represents a water quality issue of concern for public health, and so constraining the exact sources of As in the Sittaung River should be considered a priority for future research.

Limitation of Microbial Processes at Saturation-Level Salinities in a Microbial Mat Covering a Coastal Salt Flat.

Hypersaline microbial mats are dense microbial ecosystems capable of performing complete element cycling and are considered analogs of early Earth and hypothetical extraterrestrial ecosystems. We studied the functionality and limits of key biogeochemical processes, such as photosynthesis, aerobic respiration, and sulfur cycling, in salt crust-covered microbial mats from a tidal flat at the coast of Oman. We measured light, oxygen, and sulfide microprofiles as well as sulfate reduction rates at salt saturation and in flood conditions and determined fine-scale stratification of pigments, biomass, and microbial taxa in the resident microbial community. The salt crust did not protect the mats against irradiation or evaporation. Although some oxygen production was measurable at salinities of ≤30% (wt/vol) in situ, at saturation-level salinity (40%), oxygenic photosynthesis was completely inhibited and only resumed 2 days after reducing the porewater salinity to 12%. Aerobic respiration and active sulfur cycling occurred at low rates under salt saturation and increased strongly upon salinity reduction. Apart from high relative abundances of Chloroflexi, photoheterotrophic Alphaproteobacteria, Bacteroidetes, and Archaea, the mat contained a distinct layer harboring filamentous Cyanobacteria, which is unusual for such high salinities. Our results show that the diverse microbial community inhabiting this salt flat mat ultimately depends on periodic salt dilution to be self-sustaining and is rather adapted to merely survive salt saturation than to thrive under the salt crust. IMPORTANCE Due to their abilities to survive intense radiation and low water availability, hypersaline microbial mats are often suggested to be analogs of potential extraterrestrial life. However, even the limitations imposed on microbial processes by saturation-level salinity found on Earth have rarely been studied in situ. While abundance and diversity of microbial life in salt-saturated environments are well documented, most of our knowledge on process limitations stems from culture-based studies, few in situ studies, and theoretical calculations. In particular, oxygenic photosynthesis has barely been explored beyond 5 M NaCl (28% wt/vol). By applying a variety of biogeochemical and molecular methods, we show that despite abundance of photoautotrophic microorganisms, oxygenic photosynthesis is inhibited in salt-crust-covered microbial mats at saturation salinities, while rates of other energy generation processes are decreased several-fold. Hence, the complete element cycling required for self-sustaining microbial communities only occurs at lower salt concentrations.

Elements of disease in a changing world: modelling feedbacks between infectious disease and ecosystems.

An overlooked effect of ecosystem eutrophication is the potential to alter disease dynamics in primary producers, inducing disease-mediated feedbacks that alter net primary productivity and elemental recycling. Models in disease ecology rarely track organisms past death, yet death from infection can alter important ecosystem processes including elemental recycling rates and nutrient supply to living hosts. In contrast, models in ecosystem ecology rarely track disease dynamics, yet elemental nutrient pools (e.g. nitrogen, phosphorus) can regulate important disease processes including pathogen reproduction and transmission. Thus, both disease and ecosystem ecology stand to grow as fields by exploring questions that arise at their intersection. However, we currently lack a framework explicitly linking these disciplines. We developed a stoichiometric model using elemental currencies to track primary producer biomass (carbon) in vegetation and soil pools, and to track prevalence and the basic reproduction number (R0 ) of a directly transmitted pathogen. This model, parameterised for a deciduous forest, demonstrates that anthropogenic nutrient supply can interact with disease to qualitatively alter both ecosystem and disease dynamics. Using this element-focused approach, we identify knowledge gaps and generate predictions about the impact of anthropogenic nutrient supply rates on infectious disease and feedbacks to ecosystem carbon and nutrient cycling.

Colonies of marine cyanobacteria Trichodesmium interact with associated bacteria to acquire iron from dust.

Iron (Fe) bioavailability limits phytoplankton growth in vast ocean regions. Iron-rich dust uplifted from deserts is transported in the atmosphere and deposited on the ocean surface. However, this dust is a poor source of iron for most phytoplankton since dust-bound Fe is poorly soluble in seawater and dust rapidly sinks out of the photic zone. An exception is Trichodesmium, a globally important, N2 fixing, colony forming, cyanobacterium, which efficiently captures and shuffles dust to its colony core. Trichodesmium and bacteria that reside within its colonies carry out diverse metabolic interactions. Here we show evidence for mutualistic interactions between Trichodesmium and associated bacteria for utilization of iron from dust, where bacteria promote dust dissolution by producing Fe-complexing molecules (siderophores) and Trichodesmium provides dust and optimal physical settings for dissolution and uptake. Our results demonstrate how intricate relationships between producers and consumers can influence productivity in the nutrient starved open ocean.

Synergies between mycorrhizal fungi and soil microbial communities increase plant nitrogen acquisition.

Nitrogen availability often restricts primary productivity in terrestrial ecosystems. Arbuscular mycorrhizal fungi are ubiquitous symbionts of terrestrial plants and can improve plant nitrogen acquisition, but have a limited ability to access organic nitrogen. Although other soil biota mineralize organic nitrogen into bioavailable forms, they may simultaneously compete for nitrogen, with unknown consequences for plant nutrition. Here, we show that synergies between the mycorrhizal fungus Rhizophagus irregularis and soil microbial communities have a highly non-additive effect on nitrogen acquisition by the model grass Brachypodium distachyon. These multipartite microbial synergies result in a doubling of the nitrogen that mycorrhizal plants acquire from organic matter and a tenfold increase in nitrogen acquisition compared to non-mycorrhizal plants grown in the absence of soil microbial communities. This previously unquantified multipartite relationship may contribute to more than 70 Tg of annually assimilated plant nitrogen, thereby playing a critical role in global nutrient cycling and ecosystem function.

A combined lipidomic and 16S rRNA gene amplicon sequencing approach reveals archaeal sources of intact polar lipids in the stratified Black Sea water column.

Archaea are important players in marine biogeochemical cycles, and their membrane lipids are useful biomarkers in environmental and geobiological studies. However, many archaeal groups remain uncultured and their lipid composition unknown. Here, we aim to expand the knowledge on archaeal lipid biomarkers and determine the potential sources of those lipids in the water column of the euxinic Black Sea. The archaeal community was evaluated by 16S rRNA gene amplicon sequencing and by quantitative PCR. The archaeal intact polar lipids (IPLs) were investigated by ultra-high-pressure liquid chromatography coupled to high-resolution mass spectrometry. Our study revealed both a complex archaeal community and large changes with water depth in the IPL assemblages. In the oxic/upper suboxic waters (<105 m), the archaeal community was dominated by marine group (MG) I Thaumarchaeota, coinciding with a higher relative abundance of hexose phosphohexose crenarchaeol, a known marker for Thaumarchaeota. In the suboxic waters (80-110 m), MGI Nitrosopumilus sp. dominated and produced predominantly monohexose glycerol dibiphytanyl glycerol tetraethers (GDGTs) and hydroxy-GDGTs. Two clades of MGII Euryarchaeota were present in the oxic and upper suboxic zones in much lower abundances, preventing the detection of their specific IPLs. In the deep sulfidic waters (>110 m), archaea belonging to the DPANN Woesearchaeota, Bathyarchaeota, and ANME-1b clades dominated. Correlation analyses suggest that the IPLs GDGT-0, GDGT-1, and GDGT-2 with two phosphatidylglycerol (PG) head groups and archaeol with a PG, phosphatidylethanolamine, and phosphatidylserine head groups were produced by ANME-1b archaea. Bathyarchaeota represented 55% of the archaea in the deeper part of the euxinic zone and likely produces archaeol with phospho-dihexose and hexose-glucuronic acid head groups.

The complete genome sequence of Rhodobaca barguzinensis alga05 (DSM 19920) documents its adaptation for life in soda lakes.

Soda lakes, with their high salinity and high pH, pose a very challenging environment for life. Microorganisms living in these harsh conditions have had to adapt their physiology and gene inventory. Therefore, we analyzed the complete genome of the haloalkaliphilic photoheterotrophic bacterium Rhodobaca barguzinensis strain alga05. It consists of a 3,899,419 bp circular chromosome with 3624 predicted coding sequences. In contrast to most of Rhodobacterales, this strain lacks any extrachromosomal elements. To identify the genes responsible for adaptation to high pH, we compared the gene inventory in the alga05 genome with genomes of 17 reference strains belonging to order Rhodobacterales. We found that all haloalkaliphilic strains contain the mrpB gene coding for the B subunit of the MRP Na+/H+ antiporter, while this gene is absent in all non-alkaliphilic strains, which indicates its importance for adaptation to high pH. Further analysis showed that alga05 requires organic carbon sources for growth, but it also contains genes encoding the ethylmalonyl-CoA pathway for CO2 fixation. Remarkable is the genetic potential to utilize organophosphorus compounds as a source of phosphorus. In summary, its genetic inventory indicates a large flexibility of the alga05 metabolism, which is advantageous in rapidly changing environmental conditions in soda lakes.

Stable and Variable Parts of Microbial Community in Siberian Deep Subsurface Thermal Aquifer System Revealed in a Long-Term Monitoring Study.

The goal of this work was to study the diversity of microorganisms inhabiting a deep subsurface aquifer system in order to understand their functional roles and interspecies relations formed in the course of buried organic matter degradation. A microbial community of a deep subsurface thermal aquifer in the Tomsk Region, Western Siberia was monitored over the course of 5 years via a 2.7 km deep borehole 3P, drilled down to a Palaeozoic basement. The borehole water discharges with a temperature of ca. 50°C. Its chemical composition varies, but it steadily contains acetate, propionate, and traces of hydrocarbons and gives rise to microbial mats along the surface flow. Community analysis by PCR-DGGE 16S rRNA genes profiling, repeatedly performed within 5 years, revealed several dominating phylotypes consistently found in the borehole water, and highly variable diversity of prokaryotes, brought to the surface with the borehole outflow. The major planktonic components of the microbial community were Desulfovirgula thermocuniculi and Methanothermobacter spp. The composition of the minor part of the community was unstable, and molecular analysis did not reveal any regularity in its variations, except some predominance of uncultured Firmicutes. Batch cultures with complex organic substrates inoculated with water samples were set in order to enrich prokaryotes from the variable part of the community. PCR-DGGE analysis of these enrichments yielded uncultured Firmicutes, Chloroflexi, and Ignavibacteriae. A continuous-flow microaerophilic enrichment culture with a water sample amended with acetate contained Hydrogenophilus thermoluteolus, which was previously detected in the microbial mat developing at the outflow of the borehole. Cultivation results allowed us to assume that variable components of the 3P well community are hydrolytic organotrophs, degrading buried biopolymers, while the constant planktonic components of the community degrade dissolved fermentation products to methane and CO2, possibly via interspecies hydrogen transfer. Occasional washout of minor community components capable of oxygen respiration leads to the development of microbial mats at the outflow of the borehole where residual dissolved fermentation products are aerobically oxidized. Long-term community analysis with the combination of molecular and cultivation techniques allowed us to characterize stable and variable parts of the community and propose their environmental roles.

Towards a standardized Rapid Ecosystem Function Assessment (REFA).

Quantifying ecosystem functioning is important for both fundamental and applied ecological research. However, there is currently a gap between the data available and the data needed to address topical questions, such as the drivers of functioning in different ecosystems under global change or the best management to sustain provisioning of ecosystem functions and services. Here, we identify a set of important functions and propose a Rapid Ecosystem Function Assessment (REFA). The proposed methods were specifically selected to be low-tech, easy to use, repeatable, and cost efficient. Thus, REFA enables standardized and comparable measurements of proxies for these functions that can be used at a large scale within and across studies. Adopting REFA can help to close the identified ecosystem functioning data gap.