Gene Expression Changes and Community Turnover Differentially Shape the Global Ocean Metatranscriptome.

Ocean microbial communities strongly influence the biogeochemistry, food webs, and climate of our planet. Despite recent advances in understanding their taxonomic and genomic compositions, little is known about how their transcriptomes vary globally. Here, we present a dataset of 187 metatranscriptomes and 370 metagenomes from 126 globally distributed sampling stations and establish a resource of 47 million genes to study community-level transcriptomes across depth layers from pole-to-pole. We examine gene expression changes and community turnover as the underlying mechanisms shaping community transcriptomes along these axes of environmental variation and show how their individual contributions differ for multiple biogeochemically relevant processes. Furthermore, we find the relative contribution of gene expression changes to be significantly lower in polar than in non-polar waters and hypothesize that in polar regions, alterations in community activity in response to ocean warming will be driven more strongly by changes in organismal composition than by gene regulatory mechanisms. VIDEO ABSTRACT.

The Microbiology of Biological Soil Crusts.

Biological soil crusts are thin, inconspicuous communities along the soil atmosphere ecotone that, until recently, were unrecognized by ecologists and even more so by microbiologists. In its broadest meaning, the term biological soil crust (or biocrust) encompasses a variety of communities that develop on soil surfaces and are powered by photosynthetic primary producers other than higher plants: cyanobacteria, microalgae, and cryptogams like lichens and mosses. Arid land biocrusts are the most studied, but biocrusts also exist in other settings where plant development is constrained. The minimal requirement is that light impinge directly on the soil; this is impeded by the accumulation of plant litter where plants abound. Since scientists started paying attention, much has been learned about their microbial communities, their composition, ecological extent, and biogeochemical roles, about how they alter the physical behavior of soils, and even how they inform an understanding of early life on land. This has opened new avenues for ecological restoration and agriculture.

A nitrogen isotopic shift in fish otolith-bound organic matter during the Late Cretaceous.

The nitrogen isotopes of the organic matter preserved in fossil fish otoliths (ear stones) are a promising tool for reconstructing past environmental changes. We analyzed the 15N/14N ratio (δ15N) of fossil otolith-bound organic matter in Late Cretaceous fish otoliths (of Eutawichthys maastrichtiensis, Eutawichthys zideki and Pterothrissus sp.) from three deposits along the US east coast, with two of Campanian (83.6 to 77.9 Ma) and one Maastrichtian (72.1 to 66 Ma) age. δ15N and N content were insensitive to cleaning protocol and the preservation state of otolith morphological features, and N content differences among taxa were consistent across deposits, pointing to a fossil-native origin for the organic matter. All three species showed an increase in otolith-bound organic matter δ15N of ~4‰ from Campanian to Maastrichtian. As to its cause, the similar change in distinct genera argues against changing trophic level, and modern field data argue against the different locations of the sedimentary deposits. Rather, the lower δ15N in the Campanian is best interpreted as an environmental signal at the regional scale or greater, and it may be a consequence of the warmer global climate. A similar decrease has been observed in foraminifera-bound δ15N during warm periods of the Cenozoic, reflecting decreased water column denitrification and thus contraction of the ocean's oxygen deficient zones (ODZs) under warm conditions. The same δ15N-climate correlation in Cretaceous otoliths raises the prospect of an ODZ-to-climate relationship that has been consistent over the last ~80 My, applying before and after the end-Cretaceous mass extinction and spanning changes in continental configuration.

General reversal of N-decomposition relationship during long-term decomposition in boreal and temperate forests.

Decomposition of dead organic matter is fundamental to carbon (C) and nutrient cycling in terrestrial ecosystems, influencing C fluxes from the biosphere to the atmosphere. Theory predicts and evidence strongly supports that the availability of nitrogen (N) limits litter decomposition. Positive relationships between substrate N concentrations and decomposition have been embedded into ecosystem models. This decomposition paradigm, however, relies on data mostly from short-term studies analyzing controls on early-stage decomposition. We present evidence from three independent long-term decomposition investigations demonstrating that the positive N-decomposition relationship is reversed and becomes negative during later stages of decomposition. First, in a 10-y decomposition experiment across 62 woody species in a temperate forest, leaf litter with higher N concentrations exhibited faster initial decomposition rates but ended up a larger recalcitrant fraction decomposing at a near-zero rate. Second, in a 5-y N-enrichment experiment of two tree species, leaves with experimentally enriched N concentrations had faster decomposition initial rates but ultimately accumulated large slowly decomposing fractions. Measures of amino sugars on harvested litter in two experiments indicated that greater accumulation of microbial residues in N-rich substrates likely contributed to larger slowly decomposing fractions. Finally, a database of 437 measurements from 120 species in 45 boreal and temperate forest sites confirmed that higher N concentrations were associated with a larger slowly decomposing fraction. These results challenge the current treatment of interactions between N and decomposition in many ecosystems and Earth system models and suggest that even the best-supported short-term controls of biogeochemical processes might not predict long-term controls.

Negative correlation between soil salinity and soil organic carbon variability.

Soil organic carbon (SOC) is vital for terrestrial ecosystems, affecting biogeochemical processes, and soil health. It is known that soil salinity impacts SOC content, yet the specific direction and magnitude of SOC variability in relation to soil salinity remain poorly understood. Analyzing 43,459 mineral soil samples (SOC < 150 g kg-1) collected across different land covers since 1992, we approximate a soil salinity increase from 1 to 5 dS m-1 in croplands would be associated with a decline in mineral soils SOC from 0.14 g kg-1 above the mean predicted SOC ([Formula: see text] = 18.47 g kg-1) to 0.46 g kg-1 below [Formula: see text] (~-430%), while for noncroplands, such decline is sharper, from 0.96 above [Formula: see text] = 35.96 g kg-1 to 4.99 below [Formula: see text] (~-620%). Although salinity's significance in explaining SOC variability is minor (<6%), we estimate a one SD increase in salinity of topsoil samples (0 to 7 cm) correlates with respective [Formula: see text] declines of ~4.4% and ~9.26%, relative to [Formula: see text] and [Formula: see text]. The [Formula: see text] decline in croplands is greatest in vegetation/cropland mosaics while lands covered with evergreen needle-leaved trees are estimated with the highest [Formula: see text] decline in noncroplands. We identify soil nitrogen, land cover, and precipitation Seasonality Index as the most significant parameters in explaining the SOC's variability. The findings provide insights into SOC dynamics under increased soil salinity, improving understanding of SOC stock responses to land degradation and climate warming.

Phytoplankton responses to dust addition in the Fe-Mn co-limited eastern Pacific sub-Antarctic differ by source region.

The seasonal availability of light and micronutrients strongly regulates productivity in the Southern Ocean, restricting biological utilization of macronutrients and CO2 drawdown. Mineral dust flux is a key conduit for micronutrients to the Southern Ocean and a critical mediator of multimillennial-scale atmospheric CO2 oscillations. While the role of dust-borne iron (Fe) in Southern Ocean biogeochemistry has been examined in detail, manganese (Mn) availability is also emerging as a potential driver of past, present, and future Southern Ocean biogeochemistry. Here, we present results from fifteen bioassay experiments along a north-south transect in the undersampled eastern Pacific sub-Antarctic zone. In addition to widespread Fe limitation of phytoplankton photochemical efficiency, we found further responses following the addition of Mn at our southerly stations, supporting the importance of Fe-Mn co-limitation in the Southern Ocean. Moreover, addition of different Patagonian dusts resulted in enhanced photochemical efficiency with differential responses linked to source region dust characteristics in terms of relative Fe/Mn solubility. Changes in the relative magnitude of dust deposition, combined with source region mineralogy, could hence determine whether Fe or Mn limitation control Southern Ocean productivity under future as well as past climate states.

US climate policy yields water quality cobenefits in the Mississippi Basin and Gulf of Mexico.

We utilize a coupled economy-agroecology-hydrology modeling framework to capture the cascading impacts of climate change mitigation policy on agriculture and the resulting water quality cobenefits. We analyze a policy that assigns a range of United States government's social cost of carbon estimates ($51, $76, and $152/ton of CO2-equivalents) to fossil fuel-based CO2 emissions. This policy raises energy costs and, importantly for agriculture, boosts the price of nitrogen fertilizer production. At the highest carbon price, US carbon emissions are reduced by about 50%, and nitrogen fertilizer prices rise by about 90%, leading to an approximate 15% reduction in fertilizer applications for corn production across the Mississippi River Basin. Corn and soybean production declines by about 7%, increasing crop prices by 6%, while nitrate leaching declines by about 10%. Simulated nitrate export to the Gulf of Mexico decreases by 8%, ultimately shrinking the average midsummer area of the Gulf of Mexico hypoxic area by 3% and hypoxic volume by 4%. We also consider the additional benefits of restored wetlands to mitigate nitrogen loading to reduce hypoxia in the Gulf of Mexico and find a targeted wetland restoration scenario approximately doubles the effect of a low to moderate social cost of carbon. Wetland restoration alone exhibited spillover effects that increased nitrate leaching in other parts of the basin which were mitigated with the inclusion of the carbon policy. We conclude that a national climate policy aimed at reducing greenhouse gas emissions in the United States would have important water quality cobenefits.

Phosphonate production by marine microbes: Exploring new sources and potential function.

SignificancePhosphonates are a class of phosphorus metabolites characterized by a highly stable C-P bond. Phosphonates accumulate to high concentrations in seawater, fuel a large fraction of marine methane production, and serve as a source of phosphorus to microbes inhabiting nutrient-limited regions of the oligotrophic ocean. Here, we show that 15% of all bacterioplankton in the surface ocean have genes phosphonate synthesis and that most belong to the abundant groups Prochlorococcus and SAR11. Genomic and chemical evidence suggests that phosphonates are incorporated into cell-surface phosphonoglycoproteins that may act to mitigate cell mortality by grazing and viral lysis. These results underscore the large global biogeochemical impact of relatively rare but highly expressed traits in numerically abundant groups of marine bacteria.

Evidence that Pacific tuna mercury levels are driven by marine methylmercury production and anthropogenic inputs.

Pacific Ocean tuna is among the most-consumed seafood products but contains relatively high levels of the neurotoxin methylmercury. Limited observations suggest tuna mercury levels vary in space and time, yet the drivers are not well understood. Here, we map mercury concentrations in skipjack tuna across the Pacific Ocean and build generalized additive models to quantify the anthropogenic, ecological, and biogeochemical drivers. Skipjack mercury levels display a fivefold spatial gradient, with maximum concentrations in the northwest near Asia, intermediate values in the east, and the lowest levels in the west, southwest, and central Pacific. Large spatial differences can be explained by the depth of the seawater methylmercury peak near low-oxygen zones, leading to enhanced tuna mercury concentrations in regions where oxygen depletion is shallow. Despite this natural biogeochemical control, the mercury hotspot in tuna caught near Asia is explained by elevated atmospheric mercury concentrations and/or mercury river inputs to the coastal shelf. While we cannot ignore the legacy mercury contribution from other regions to the Pacific Ocean (e.g., North America and Europe), our results suggest that recent anthropogenic mercury release, which is currently largest in Asia, contributes directly to present-day human mercury exposure.

Loss of grazing by large mammalian herbivores can destabilize the soil carbon pool.

Grazing by mammalian herbivores can be a climate mitigation strategy as it influences the size and stability of a large soil carbon (soil-C) pool (more than 500 Pg C in the world's grasslands, steppes, and savannas). With continuing declines in the numbers of large mammalian herbivores, the resultant loss in grazer functions can be consequential for this soil-C pool and ultimately for the global carbon cycle. While herbivore effects on the size of the soil-C pool and the conditions under which they lead to gain or loss in soil-C are becoming increasingly clear, their effect on the equally important aspect of stability of soil-C remains unknown. We used a replicated long-term field experiment in the Trans-Himalayan grazing ecosystem to evaluate the consequences of herbivore exclusion on interannual fluctuations in soil-C (2006 to 2021). Interannual fluctuations in soil-C and soil-N were 30 to 40% higher after herbivore exclusion than under grazing. Structural equation modeling suggested that grazing appears to mediate the stabilizing versus destabilizing influences of nitrogen (N) on soil-C. This may explain why N addition stimulates soil-C loss in the absence of herbivores around the world. Herbivore loss, and the consequent decline in grazer functions, can therefore undermine the stability of soil-C. Soil-C is not inert but a very dynamic pool. It can provide nature-based climate solutions by conserving and restoring a functional role of large mammalian herbivores that extends to the stoichiometric coupling between soil-C and soil-N.

Biogeochemical fingerprinting of magnetotactic bacterial magnetite.

Biominerals are important archives of the presence of life and environmental processes in the geological record. However, ascribing a clear biogenic nature to minerals with nanometer-sized dimensions has proven challenging. Identifying hallmark features of biologically controlled mineralization is particularly important for the case of magnetite crystals, resembling those produced by magnetotactic bacteria (MTB), which have been used as evidence of early prokaryotic life on Earth and in meteorites. We show here that magnetite produced by MTB displays a clear coupled C-N signal that is absent in abiogenic and/or biomimetic (protein-mediated) nanometer-sized magnetite. We attribute the presence of this signal to intracrystalline organic components associated with proteins involved in magnetosome formation by MTB. These results demonstrate that we can assign a biogenic origin to nanometer-sized magnetite crystals, and potentially other biominerals of similar dimensions, using unique geochemical signatures directly measured at the nanoscale. This finding is significant for searching for the earliest presence of life in the Earth's geological record and prokaryotic life on other planets.

The biological carbon pump in CMIP6 models: 21st century trends and uncertainties.

The biological carbon pump (BCP) stores ∼1,700 Pg C from the atmosphere in the ocean interior, but the magnitude and direction of future changes in carbon sequestration by the BCP are uncertain. We quantify global trends in export production, sinking organic carbon fluxes, and sequestered carbon in the latest Coupled Model Intercomparison Project Phase 6 (CMIP6) future projections, finding a consistent 19 to 48 Pg C increase in carbon sequestration over the 21st century for the SSP3-7.0 scenario, equivalent to 5 to 17% of the total increase of carbon in the ocean by 2100. This is in contrast to a global decrease in export production of -0.15 to -1.44 Pg C y-1. However, there is significant uncertainty in the modeled future fluxes of organic carbon to the deep ocean associated with a range of different processes resolved across models. We demonstrate that organic carbon fluxes at 1,000 m are a good predictor of long-term carbon sequestration and suggest this is an important metric of the BCP that should be prioritized in future model studies.

The importance of hydrology in routing terrestrial carbon to the atmosphere via global streams and rivers.

SignificanceStream/river carbon dioxide (CO2) emission has significant spatial and seasonal variations critical for understanding its macroecosystem controls and plumbing of the terrestrial carbon budget. We relied on direct fluvial CO2 partial pressure measurements and seasonally varying gas transfer velocity and river network surface area estimates to resolve reach-level seasonal variations of the flux at the global scale. The percentage of terrestrial primary production (GPP) shunted into rivers that ultimately contributes to CO2 evasion increases with discharge across regions, due to a stronger response in fluvial CO2 evasion to discharge than GPP. This highlights the importance of hydrology, in particular water throughput, in terrestrial-fluvial carbon transfers and the need to account for this effect in plumbing the terrestrial carbon budget.

Diversity in the utilization of different molecular classes of dissolved organic matter by heterotrophic marine bacteria.

Heterotrophic marine bacteria utilize and recycle dissolved organic matter (DOM), impacting biogeochemical cycles. It is currently unclear to what extent distinct DOM components can be used by different heterotrophic clades. Here, we ask how a natural microbial community from the Eastern Mediterranean Sea (EMS) responds to different molecular classes of DOM (peptides, amino acids, amino sugars, disaccharides, monosaccharides, and organic acids) comprising much of the biomass of living organisms. Bulk bacterial activity increased after 24 h for all treatments relative to the control, while glucose and ATP uptake decreased or remained unchanged. Moreover, while the per-cell uptake rate of glucose and ATP decreased, that of Leucin significantly increased for amino acids, reflecting their importance as common metabolic currencies in the marine environment. Pseudoalteromonadaceae dominated the peptides treatment, while different Vibrionaceae strains became dominant in response to amino acids and amino sugars. Marinomonadaceae grew well on organic acids, and Alteromonadaseae on disaccharides. A comparison with a recent laboratory-based study reveals similar peptide preferences for Pseudoalteromonadaceae, while Alteromonadaceae, for example, grew well in the lab on many substrates but dominated in seawater samples only when disaccharides were added. We further demonstrate a potential correlation between the genetic capacity for degrading amino sugars and the dominance of specific clades in these treatments. These results highlight the diversity in DOM utilization among heterotrophic bacteria and complexities in the response of natural communities. IMPORTANCE: A major goal of microbial ecology is to predict the dynamics of natural communities based on the identity of the organisms, their physiological traits, and their genomes. Our results show that several clades of heterotrophic bacteria each grow in response to one or more specific classes of organic matter. For some clades, but not others, growth in a complex community is similar to that of isolated strains in laboratory monoculture. Additionally, by measuring how the entire community responds to various classes of organic matter, we show that these results are ecologically relevant, and propose that some of these resources are utilized through common uptake pathways. Tracing the path between different resources to the specific microbes that utilize them, and identifying commonalities and differences between different natural communities and between them and lab cultures, is an important step toward understanding microbial community dynamics and predicting how communities will respond to perturbations.

Nematodes alter the taxonomic and functional profiles of benthic bacterial communities: A metatranscriptomic approach.

Marine sediments cover 70% of the Earth's surface, and harbour diverse bacterial communities critical for marine biogeochemical processes, which affect climate change, biodiversity and ecosystem functioning. Nematodes, the most abundant and species-rich metazoan organisms in marine sediments, in turn, affect benthic bacterial communities and bacterial-mediated ecological processes, but the underlying mechanisms by which they affect biogeochemical cycles remain poorly understood. Here, we demonstrate using a metatranscriptomic approach that nematodes alter the taxonomic and functional profiles of benthic bacterial communities. We found particularly strong stimulation of nitrogen-fixing and methane-oxidizing bacteria in the presence of nematodes, as well as increased functional activity associated with methane metabolism and degradation of various carbon compounds. This study provides empirical evidence that the presence of nematodes results in taxonomic and functional shifts in active bacterial communities, indicating that nematodes may play an important role in benthic ecosystem processes.

Microbial evolution-An under-appreciated driver of soil carbon cycling.

Although substantial advances in predicting the ecological impacts of global change have been made, predictions of the evolutionary impacts have lagged behind. In soil ecosystems, microbes act as the primary energetic drivers of carbon cycling; however, microbes are also capable of evolving on timescales comparable to rates of global change. Given the importance of soil ecosystems in global carbon cycling, we assess the potential impact of microbial evolution on carbon-climate feedbacks in this system. We begin by reviewing the current state of knowledge concerning microbial evolution in response to global change and its specific effect on soil carbon dynamics. Through this integration, we synthesize a roadmap detailing how to integrate microbial evolution into ecosystem biogeochemical models. Specifically, we highlight the importance of microscale mechanistic soil carbon models, including choosing an appropriate evolutionary model (e.g., adaptive dynamics, quantitative genetics), validating model predictions with 'omics' and experimental data, scaling microbial adaptations to ecosystem level processes, and validating with ecosystem-scale measurements. The proposed steps will require significant investment of scientific resources and might require 10-20 years to be fully implemented. However, through the application of multi-scale integrated approaches, we will advance the integration of microbial evolution into predictive understanding of ecosystems, providing clarity on its role and impact within the broader context of environmental change.

Ocean deoxygenation caused non-linear responses in the structure and functioning of benthic ecosystems.

The O2 content of the global ocean has been declining progressively over the past decades, mainly because of human activities and global warming. Nevertheless, how long-term deoxygenation affects macrobenthic communities, sediment biogeochemistry and their mutual feedback remains poorly understood. Here, we evaluate the response of the benthic assemblages and biogeochemical functioning to decreasing O2 concentrations along the persistent bottom-water dissolved O2 gradient of the Estuary and Gulf of St. Lawrence (QC, Canada). We report several of non-linear biodiversity and functional responses to decreasing O2 concentrations, and identify an O2 threshold that occurs at approximately at 63 µM. Below this threshold, macrobenthic community assemblages change, and bioturbation rates drastically decrease to near zero. Consequently, the sequence of electron acceptors used to metabolize the sedimentary organic matter is squeezed towards the sediment surface while reduced compounds accumulate closer (as much as 0.5-2.5 cm depending on the compound) to the sediment-water interface. Our results illustrate the capacity of bioturbating species to compensate for the biogeochemical consequences of hypoxia and can help to predict future changes in benthic ecosystems.

Les teneurs en O2 de l'océan mondial ont diminué progressivement au cours des dernières décennies, principalement en raison des activités humaines et du réchauffement climatique. Néanmoins, les effets à long terme de la désoxygénation sur les communautés macrobenthiques, la biogéochimie des sédiments et leurs interactions mutuelles demeurent mal compris. Dans cette étude, nous évaluons la réponse des assemblages de macrofaune benthiques et de la dynamique biogéochimique sédimentaire aux concentrations décroissantes d'O2 le long du gradient persistant d'O2 dissous dans l'eau de fond de l'estuaire et du golfe du Saint-Laurent (QC, Canada). Nous avons observé plusieurs réponses non linéaires de la biodiversité et de la dynamique biogéochimique sédimentaire face à la diminution de la concentration en O2 avec un seuil situé à environ 63 µM. En dessous de ce seuil, les assemblages de communautés macrobenthiques changent, et les taux de bioturbation diminuent drastiquement pour atteindre des niveaux presque nuls. En conséquence, la séquence des accepteurs d'électrons utilisés pour minéraliser la matière organique sédimentaire se contracte vers la surface du sédiment, tandis que les composés réduits s'accumulent plus près (jusqu'à 0.5 à 2.5 cm selon le composé) de l'interface sédiment-eau. Nos résultats illustrent la capacité des espèces bioturbatrices à compenser les conséquences biogéochimiques de la désoxygénation et peuvent contribuer à prédire les futurs changements dans les écosystèmes benthiques.

Shifts in bacterial traits under chronic nitrogen deposition align with soil processes in arbuscular, but not ectomycorrhizal-associated trees.

Nitrogen (N) deposition increases soil carbon (C) storage by reducing microbial activity. These effects vary in soil beneath trees that associate with arbuscular (AM) and ectomycorrhizal (ECM) fungi. Variation in carbon C and N uptake traits among microbes may explain differences in soil nutrient cycling between mycorrhizal associations in response to high N loads, a mechanism not previously examined due to methodological limitations. Here, we used quantitative Stable Isotope Probing (qSIP) to measure bacterial C and N assimilation rates from an added organic compound, which we conceptualize as functional traits. As such, we applied a trait-based approach to explore whether variation in assimilation rates of bacterial taxa can inform shifts in soil function under chronic N deposition. We show taxon-specific and community-wide declines of bacterial C and N uptake under chronic N deposition in both AM and ECM soils. N deposition-induced reductions in microbial activity were mirrored by declines in soil organic matter mineralization rates in AM but not ECM soils. Our findings suggest C and N uptake traits of bacterial communities can predict C cycling feedbacks to N deposition in AM soils, but additional data, for instance on the traits of fungi, may be needed to connect microbial traits with soil C and N cycling in ECM systems. Our study also highlights the potential of employing qSIP in conjunction with trait-based analytical approaches to inform how ecological processes of microbial communities influence soil functioning.