Soil Geobacteraceae are the key predictors of neurotoxic methylmercury bioaccumulation in rice.

Contamination of rice by the potent neurotoxin methylmercury (MeHg) originates from microbe-mediated Hg methylation in soils. However, the high diversity of Hg methylating microorganisms in soils hinders the prediction of MeHg formation and challenges the mitigation of MeHg bioaccumulation via regulating soil microbiomes. Here we explored the roles of various cropland microbial communities in MeHg formation in the potentials leading to MeHg accumulation in rice and reveal that Geobacteraceae are the key predictors of MeHg bioaccumulation in paddy soil systems. We characterized Hg methylating microorganisms from 67 cropland ecosystems across 3,600 latitudinal kilometres. The simulations of a rice-paddy biogeochemical model show that MeHg accumulation in rice is 1.3-1.7-fold more sensitive to changes in the relative abundance of Geobacteraceae compared to Hg input, which is recognized as the primary parameter in controlling MeHg exposure. These findings open up a window to predict MeHg formation and accumulation in human food webs, enabling more efficient mitigation of risks to human health through regulations of key soil microbiomes.

Assessing microbial degradation potential of methylmercury in different types of paddy soil through short-term incubation.

The neurotoxic methylmercury (MeHg) in paddy soils can accumulate in rice grains. Microbial demethylation is an important pathway of MeHg degradation in soil, but the effect of soil type on microbial degradation of MeHg remains unclear. Therefore, we investigated MeHg degradation in eight typical paddy soils and analyzed the associations between soil physiochemical properties and microbial degradation efficiencies of MeHg. Results showed that MeHg was significantly degraded in unsterilized paddy soils, and the microbial degradation efficiency ranged from 10.8% to 64.6% after a 30-day incubation. The high microbial degradation efficiency of MeHg was observed in the soils with high levels of clay content, whereas relatively low degradation efficiency was found in the red paddy soils. We identified that Paenibacillaceae was the most important microbial predictor of MeHg degradation and was positively correlated with the degradation efficiency in the soils. The abundances of these microbial taxa associated with MeHg degradation were positively correlated with clay content. In addition, Eh, pH, and SOC could influence microbial degradation of MeHg by regulating certain microbial communities. Our results indicate that soil type is crucial in driving MeHg degradation, which has important implications for the mitigation of MeHg pollution in various croplands.

Soil contamination in nearby natural areas mirrors that in urban greenspaces worldwide.

Soil contamination is one of the main threats to ecosystem health and sustainability. Yet little is known about the extent to which soil contaminants differ between urban greenspaces and natural ecosystems. Here we show that urban greenspaces and adjacent natural areas (i.e., natural/semi-natural ecosystems) shared similar levels of multiple soil contaminants (metal(loid)s, pesticides, microplastics, and antibiotic resistance genes) across the globe. We reveal that human influence explained many forms of soil contamination worldwide. Socio-economic factors were integral to explaining the occurrence of soil contaminants worldwide. We further show that increased levels of multiple soil contaminants were linked with changes in microbial traits including genes associated with environmental stress resistance, nutrient cycling, and pathogenesis. Taken together, our work demonstrates that human-driven soil contamination in nearby natural areas mirrors that in urban greenspaces globally, and highlights that soil contaminants have the potential to cause dire consequences for ecosystem sustainability and human wellbeing.

Methylmercury Degradation by Trivalent Manganese.

Methylmercury (MeHg) is a potent neurotoxin and has great adverse health impacts on humans. Organisms and sunlight-mediated demethylation are well-known detoxification pathways of MeHg, yet whether abiotic environmental components contribute to MeHg degradation remains poorly known. Here, we report that MeHg can be degraded by trivalent manganese (Mn(III)), a naturally occurring and widespread oxidant. We found that 28 ± 4% MeHg could be degraded by Mn(III) located on synthesized Mn dioxide (MnO2-x) surfaces during the reaction of 0.91 µg·L-1 MeHg and 5 g·L-1 mineral at an initial pH of 6.0 for 12 h in 10 mM NaNO3 at 25 °C. The presence of low-molecular-weight organic acids (e.g., oxalate and citrate) substantially enhances MeHg degradation by MnO2-x via the formation of soluble Mn(III)-ligand complexes, leading to the cleavage of the carbon-Hg bond. MeHg can also be degraded by reactions with Mn(III)-pyrophosphate complexes, with apparent degradation rate constants comparable to those by biotic and photolytic degradation. Thiol ligands (cysteine and glutathione) show negligible effects on MeHg demethylation by Mn(III). This research demonstrates potential roles of Mn(III) in degrading MeHg in natural environments, which may be further explored for remediating heavily polluted soils and engineered systems containing MeHg.

Potential for mercury methylation by Asgard archaea in mangrove sediments.

Methylmercury (MeHg) is a potent neurotoxin that bioaccumulates along food chains. The conversion of MeHg from mercury (Hg) is mediated by a variety of anaerobic microorganisms carrying hgcAB genes. Mangrove sediments are potential hotspots of microbial Hg methylation; however, the microorganisms responsible for Hg methylation are poorly understood. Here, we conducted metagenomic and metatranscriptomic analyses to investigate the diversity and distribution of putative microbial Hg-methylators in mangrove ecosystems. The highest hgcA abundance and expression occurred in surface sediments in Shenzhen, where the highest MeHg concentration was also observed. We reconstructed 157 metagenome-assembled genomes (MAGs) carrying hgcA and identified several putative novel Hg-methylators, including one Asgard archaea (Lokiarchaeota). Further analysis of MAGs revealed that Deltaproteobacteria, Euryarchaeota, Bacteroidetes, Chloroflexi, and Lokiarchaeota were the most abundant and active Hg-methylating groups, implying their crucial role in MeHg production. By screening publicly available MAGs, 104 additional Asgard MAGs carrying hgcA genes were identified from a wide range of coast, marine, permafrost, and lake sediments. Protein homology modelling predicts that Lokiarchaeota HgcAB proteins contained the highly conserved amino acid sequences and folding structures required for Hg methylation. Phylogenetic tree revealed that hgcA genes from Asgard clustered with fused hgcAB genes, indicating a transitional stage of Asgard hgcA genes. Our findings thus suggest that Asgard archaea are potential novel Hg-methylating microorganisms and play an important role in hgcA evolution.

Soil biodiversity supports the delivery of multiple ecosystem functions in urban greenspaces.

While the contribution of biodiversity to supporting multiple ecosystem functions is well established in natural ecosystems, the relationship of the above- and below-ground diversity with ecosystem multifunctionality remains virtually unknown in urban greenspaces. Here we conducted a standardized survey of urban greenspaces from 56 municipalities across six continents, aiming to investigate the relationships of plant and soil biodiversity (diversity of bacteria, fungi, protists and invertebrates, and metagenomics-based functional diversity) with 18 surrogates of ecosystem functions from nine ecosystem services. We found that soil biodiversity across biomes was significantly and positively correlated with multiple dimensions of ecosystem functions, and contributed to key ecosystem services such as microbially driven carbon pools, organic matter decomposition, plant productivity, nutrient cycling, water regulation, plant-soil mutualism, plant pathogen control and antibiotic resistance regulation. Plant diversity only indirectly influenced multifunctionality in urban greenspaces via changes in soil conditions that were associated with soil biodiversity. These findings were maintained after controlling for climate, spatial context, soil properties, vegetation and management practices. This study provides solid evidence that conserving soil biodiversity in urban greenspaces is key to supporting multiple dimensions of ecosystem functioning, which is critical for the sustainability of urban ecosystems and human wellbeing.

Global hotspots for soil nature conservation.

Soils are the foundation of all terrestrial ecosystems1. However, unlike for plants and animals, a global assessment of hotspots for soil nature conservation is still lacking2. This hampers our ability to establish nature conservation priorities for the multiple dimensions that support the soil system: from soil biodiversity to ecosystem services. Here, to identify global hotspots for soil nature conservation, we performed a global field survey that includes observations of biodiversity (archaea, bacteria, fungi, protists and invertebrates) and functions (critical for six ecosystem services) in 615 composite samples of topsoil from a standardized survey in all continents. We found that each of the different ecological dimensions of soils-that is, species richness (alpha diversity, measured as amplicon sequence variants), community dissimilarity and ecosystem services-peaked in contrasting regions of the planet, and were associated with different environmental factors. Temperate ecosystems showed the highest species richness, whereas community dissimilarity peaked in the tropics, and colder high-latitudinal ecosystems were identified as hotspots of ecosystem services. These findings highlight the complexities that are involved in simultaneously protecting multiple ecological dimensions of soil. We further show that most of these hotspots are not adequately covered by protected areas (more than 70%), and are vulnerable in the context of several scenarios of global change. Our global estimation of priorities for soil nature conservation highlights the importance of accounting for the multidimensionality of soil biodiversity and ecosystem services to conserve soils for future generations.

Increased water inputs fuel microbial mercury methylation in upland soils.

Mercury (Hg) can be converted to neurotoxic methylmercury (MeHg) by certain microbes typically in anaerobic environments, threatening human health due to its bioaccumulation in food webs. However, it is unclear whether and how Hg can be methylated in legacy aerobic uplands with increasing water. Here, we conducted a series of incubation experiments to investigate the effects of increased water content on MeHg production in two typical upland soils (i.e., long-term and short-term use). Results showed that marked MeHg production occurred in water-saturated upland soils, which was strongly correlated with the proportions of significantly stimulated Hg methylating taxon (i.e., Geobacter). Elevated temperature further enhanced MeHg production by blooming proportions of typical Hg methylators (i.e., Clostridium, Acetonema, and Geobacter). Water saturation could also enhance microbial Hg methylation by facilitating microbial syntrophy between non-Hg methylators and Hg methylators. Taken together, the present work suggests that uplands could turn into a potential MeHg reservoir in response to water inputs resulting from rainfall or anthropogenic irrigation.

[Characteristics and Assessment of Heavy Metal Contamination in Soils of Industrial Regions in the Yangtze River Economic Belt].

The Yangtze River Economic Belt is one of the areas with rapid economic development in China, although the intensive industrial activities have aggravated the emissions of soil pollutants in this area. Industrial activities are important sources of soil heavy metal contamination; however, the spatial distribution and main emission sources of soil heavy metal contamination in industrial regions of the economic belt remain unclear. Here, we collected data on the concentrations of eight heavy metals (Cd, Cr, Cu, Pb, Ni, Hg, As, and Zn) in the surface soils of 193 industrial regions covering 11 provinces and cities of the Yangtze River Economic Belt from China National Knowledge Infrastructure (CNKI), Web of Science, and other public databases. On this basis, we analyzed the spatial distribution characteristics of heavy metals and the contamination characteristics of typical industries. The results showed that the heavy metal contamination in agricultural land was more serious than that in industrial land. A total of 58.49%, 39.53%, and 22.64% of the agricultural land, respectively, contained levels of Cd, Zn, and Pb that exceeded the screening values of the Soil Environmental Quality Control Standard for Soil Pollution Risk of Agricultural Land (GB 15618-2018). The results of geo-accumulation index analysis showed that the contamination degree of the eight heavy metals was in the order of Cd (2.52)>Hg (1.17)>Pb (1.00)>Zn (0.90)>Cu (0.72)>As (0.02)>Cr (-0.40)>Ni(-0.48). As for the spatial distribution, Hg, Cd, As, Cu, Pb, and Zn were the main pollutants in the upstream and middle reaches of the industrial regions, whereas As, Cd, and Hg were the main pollutants in the downstream industrial regions. Different types of industry caused different types of contamination. Mining industries caused the most serious soil contamination, the main pollutants of which were Hg and Cd, followed by Cu, Pb, and Zn. Furthermore, metal processing industries mainly caused Cd and Pb contamination. The surrounding soils of chemical industries were contamination-free or only slightly polluted by the eight heavy metals, whereas petroleum processing industries mainly caused Cd contamination. Our study provides important theoretical basis for the future prevention and control of soil heavy metal contamination in industrial regions of the Yangtze River Economic Belt.

Important Roles of Thiols in Methylmercury Uptake and Translocation by Rice Plants.

The bioaccumulation of the neurotoxin methylmercury (MeHg) in rice is a significant concern due to its potential risk to humans. Thiols have been known to affect MeHg bioavailability in microorganisms, but how thiols influence MeHg accumulation in rice plants remains unknown. Here, we investigated effects of common low-molecular-weight thiols, including cysteine (Cys), glutathione (GSH), and penicillamine (PEN), on MeHg uptake and translocation by rice plants. Results show that rice roots can rapidly take up MeHg, and this process is influenced by the types and concentrations of thiols in the system. The presence of Cys facilitated MeHg uptake by roots and translocation to shoots, while GSH could only promote MeHg uptake, but not translocation, by roots. Conversely, PEN significantly inhibited MeHg uptake and translocation to shoots. Using labeled 13Cys assays, we also found that MeHg uptake was coupled with Cys accumulation in rice roots. Moreover, analyses of comparative transcriptomics revealed that key genes associated with metallothionein and SULTR transporter families may be involved in MeHg uptake. These findings provide new insights into the uptake and translocation of MeHg in rice plants and suggest potential roles of thiol attributes in affecting MeHg bioavailability and bioaccumulation in rice.

Microbial assemblies associated with temperature sensitivity of soil respiration along an altitudinal gradient.

Identifying the drivers of the response of soil microbial respiration to warming is integral to accurately forecasting the carbon-climate feedbacks in terrestrial ecosystems. Microorganisms are the fundamental drivers of soil microbial respiration and its response to warming; however, the specific microbial communities and properties involved in the process remain largely undetermined. Here, we identified the associations between microbial community and temperature sensitivity (Q10) of soil microbial respiration in alpine forests along an altitudinal gradient (from 2974 to 3558 m) from the climate-sensitive Tibetan Plateau. Our results showed that changes in microbial community composition accounted for more variations of Q10 values than a wide range of other factors, including soil pH, moisture, substrate quantity and quality, microbial biomass, diversity and enzyme activities. Specifically, co-occurring microbial assemblies (i.e., ecological clusters or modules) targeting labile carbon consumption were negatively correlated with Q10 of soil microbial respiration, whereas microbial assemblies associated with recalcitrant carbon decomposition were positively correlated with Q10 of soil microbial respiration. Furthermore, there were progressive shifts of microbial assemblies from labile to recalcitrant carbon consumption along the altitudinal gradient, supporting relatively high Q10 values in high-altitude regions. Our results provide new insights into the link between changes in major microbial assemblies with different trophic strategies and Q10 of soil microbial respiration along an altitudinal gradient, highlighting that warming could have stronger effects on microbially-mediated soil organic matter decomposition in high-altitude regions than previously thought.

Global homogenization of the structure and function in the soil microbiome of urban greenspaces.

The structure and function of the soil microbiome of urban greenspaces remain largely undetermined. We conducted a global field survey in urban greenspaces and neighboring natural ecosystems across 56 cities from six continents, and found that urban soils are important hotspots for soil bacterial, protist and functional gene diversity, but support highly homogenized microbial communities worldwide. Urban greenspaces had a greater proportion of fast-growing bacteria, algae, amoebae, and fungal pathogens, but a lower proportion of ectomycorrhizal fungi than natural ecosystems. These urban ecosystems also showed higher proportions of genes associated with human pathogens, greenhouse gas emissions, faster nutrient cycling, and more intense abiotic stress than natural environments. City affluence, management practices, and climate were fundamental drivers of urban soil communities. Our work paves the way toward a more comprehensive global-scale perspective on urban greenspaces, which is integral to managing the health of these ecosystems and the well-being of human populations.

Soil microbial trait-based strategies drive metabolic efficiency along an altitude gradient.

Trait-based approaches provide a candidate framework for linking soil microbial community to ecosystem processes, yet how the trade-offs in different microbial traits regulate the community-level metabolic efficiency remains unknown. Herein we assessed the roles of the microbial taxa with particular trait strategies in mediating soil microbial metabolic efficiency along an altitude gradient on the Tibetan Plateau. Results showed that soil microbial metabolic efficiency declined with increasing altitude, as indicated by the increasing metabolic quotient (microbial respiration per unit biomass, qCO2) and decreasing carbon use efficiency (CUE). Both qCO2 and CUE were predominantly predicted by microbial physiological and taxonomic attributes after considering key environmental factors including soil pH, substrate quantity and quality. Specifically, the reduced metabolic efficiency was associated with higher investment into nutrient (particularly for phosphorus) acquisitions via enzymes. Furthermore, we identified key microbial assemblies selected by harsh environments (low substrate quality and temperature) as important predictors of metabolic efficiency. These results suggest that particular microbial assemblies adapted to nutrient limited and cold habitats, but at the expense of lower metabolic efficient at higher altitude. Our findings provide a candidate mechanism underlying community-level metabolic efficiency, which has important implications for microbial-mediated processes such as carbon dynamics under global climate changes.

Microbial Communities Associated with Methylmercury Degradation in Paddy Soils.

Bioaccumulation of the neurotoxin methylmercury (MeHg) in rice has raised worldwide concerns because of its risks to human health. Certain microorganisms are able to degrade MeHg in pure cultures, but the roles and diversities of the microbial communities in MeHg degradation in rice paddy soils are unknown. Using a series of microcosms, we investigated MeHg degradation in paddy soils from Hunan, Guizhou, and Hubei provinces, representing three major rice production regions in China, and further characterized one of the soils from the Hunan Province for microbial communities associated with MeHg degradation. Microbial demethylation was observed in all three soils, demonstrated by significantly more MeHg degraded in the unsterilized soils than in the sterilized controls. More demethylation occurred in water-saturated soils than in unsaturated soils, but the addition of molybdate and bromoethanesulfonic acid as the respective inhibitors of sulfate reducing bacteria and methanogens showed insignificant effects on MeHg degradation. However, the addition of Cu enhanced MeHg degradation and the enrichment of Xanthomonadaceae in the unsaturated soil. 16S rRNA Illumina sequencing and metatranscriptomic analyses of the Hunan soil consistently revealed that Catenulisporaceae, Frankiaceae, Mycobacteriaceae, and Thermomonosporaceae were among the most likely microbial taxa in influencing MeHg degradation in the paddy soil, and they were confirmed by combined analyses of the co-occurrence network, random forest modeling, and linear discriminant analysis of the effect size. Our results shed additional light onto the roles of microbial communities in MeHg degradation in paddy soils and its subsequent bioaccumulation in rice grains.

[Effects of Wetland Types on Distribution of Soil Methylmercury Based on the Region of Nanweng River in the Greater Xing'an Mountains].

Methylmercury (MeHg) is the most toxic organic matter of all mercury (Hg) compounds. Its toxicity is far higher than that of inorganic Hg. Methylmercury can enter the human body through food, threatening human health. Based on the Nanweng River National Nature Reserve in the Greater Xing'an Mountains, the differences in the distribution of MeHg in soil samples collected from four types of wetlands, including medium swamp, low swamp, island forest, and forest soil, and the effect of the soil properties on the MeHg content were investigated in this study. The results show that:① the trends of the total Hg and MeHg levels are inconsistent. The order of the mean total Hg content is island forest (138.76 mg·kg-1±101.97 mg·kg-1) > forest soil (117.57 mg·kg-1±32.44 mg·kg-1) > low swamp (71.8 mg·kg-1±1.42 mg·kg-1) > median swamp (65.11 mg·kg-1±26.69 mg·kg-1), while the mean MeHg content is in the order of island forest (1.14 µg·kg-1±1.15 µg·kg-1) > medium swamp (0.87 µg·kg-1±1.06 µg·kg-1) > low swamp (0.28 µg·kg-1±0.06 µg·kg-1) > forest soil (0.1 µg·kg-1±0.05 µg·kg-1); ② the contents of MeHg in the island forest and medium swamp were relatively high and fluctuated dramatically, whereas the contents of MeHg in the low swamp and forest soil were lower and showed little change between each sampling point; ③ the longer the marsh wetland formation was, the higher was the MeHg content, that is, median swamp (0.87 µg·kg-1±1.06 µg·kg-1) > low swamp (0.28 µg·kg-1±0.06 µg·kg-1); the soil pH was positively correlated with MeHg (P<0.05); in the medium swamp area, the content of MeHg was positively related to the water content (WC), organic matter (OM%), carbon (C%), and total mercury (THg; P<0.05); in the island forest areas, the MeHg content showed a linear relationship with the soil pH and NH4+-N (P<0.05). This study reveals the distribution characteristics of MeHg and its influencing factors for different wetland ecosystems, providing data supporting the comprehensive evaluation of MeHg accumulation in wetland ecosystems.