Plant diversity and density predict belowground diversity and function in an early successional alpine ecosystem.

Despite decades of interest, few studies have provided evidence supporting theoretical expectations for coupled relationships between aboveground and belowground diversity and ecosystem functioning in non-manipulated natural ecosystems. We characterized plant species richness and density, soil bacterial, fungal and eukaryotic species richness and phylogenetic diversity (using 16S, ITS, and 18S gene sequencing), and ecosystem function (levels of soil C and N, and rates of microbial enzyme activities) along a natural gradient in plant richness and density in high-elevation, C-deficient soils to examine the coupling between above- and belowground systems. Overall, we observed a strong positive relationship between aboveground (plant richness and density) and belowground (bacteria, fungi, and non-fungal eukaryotes) richness. In addition to the correlations between plants and soil communities, C and N pools, and rates of enzyme activities increased as plant and soil communities became richer and more diverse. Our results suggest that the theoretically expected positive correlation between above- and belowground communities does exist in natural systems, but may be undetectable in late successional ecosystems due to the buildup of legacy organic matter that results in extremely complex belowground communities. In contrast, microbial communities in early successional systems, such as the system described here, are more directly dependent on contemporary inputs from plants and therefore are strongly correlated with plant diversity and density.

Limited ecosystem recovery from simulated chronic nitrogen deposition.

The realization that anthropogenic nitrogen (N) deposition is causing significant environmental change in many ecosystems has led to lower emissions of reactive N and deposition rates in many regions. However, the impacts of N deposition on terrestrial ecosystems can be long lasting, with significant inertia in the return of the biota and biogeochemical processes to baseline levels. To better understand patterns of recovery and the factors that may contribute to slow or no responses following declines in N deposition, we followed plant species composition, microbial abundance, N cycling rates, soil pH, and pools of NO3- and extractable cations in an impacted alpine ecosystem following cessation of 12-yr experiment increasing N deposition rates by 0, 20, 40, and 60 kg N·ha-1 ·yr-1 . Simulated N deposition had resulted in a tripling in the cover of the nitrophilic species Carex rupestris, while the dominant sedge Kobresia myosuroides had decreased by more than half at the highest N input level. In addition, nitrification rates were elevated, soil extractable magnesium (Mg2+ ) and pH decreased, and aluminum (Al3+ ) and manganese (Mn2+ ) were elevated at the highest N treatment inputs. Over the nine years following cessation of N additions to the impacted plots, only the cover of the nitrophilic C. rupestris showed any recovery to prior levels. Abundances of both bacteria and fungi were lower with N addition in both treatment and recovery plots. Rates of nitrification and pools of NO3- remained elevated in the recovery plots, likely contributing to the lack of biotic response to the cessation of N inputs. In addition, nutrient base cations (Ca2+ and Mg2+ ) and soil pH remained depressed, and the toxic metal cations (Al3+ and Mn2+ ) remained elevated in recovery plots, also potentially influencing biotic recovery. These results emphasize the importance of considering long-term environmental impacts of N deposition associated with legacy effects, such as elevated N cycling and losses of base cations, in determining environmental standards such as the metrics used for critical loads.

Rapid temporal changes in root colonization by arbuscular mycorrhizal fungi and fine root endophytes, not dark septate endophytes, track plant activity and environment in an alpine ecosystem.

Fungal root endophytes play an important role in plant nutrition, helping plants acquire nutrients in exchange for photosynthates. We sought to characterize the progression of root colonization by arbuscular mycorrhizal fungi (AMF), dark septate endophytes (DSE), and fine root endophytes (FRE) over an alpine growing season, and to understand the role of the host plant and environment in driving colonization levels. We sampled four forbs on a regular schedule from June 26th-September 11th from a moist meadow (3535 m a.s.l) on Niwot Ridge, Rocky Mountain Front Range, CO, USA. We quantified the degree of root colonization by storage structures, exchange structures, and hyphae of all three groups of fungi. AMF and FRE percent colonization fluctuated significantly over time, while DSE did not. All AMF structures changed over time, and the degree of change in vesicles differed by plant species. FRE hyphae, AMF arbuscules and AMF vesicles peaked late in the season as plants produced seeds. AMF hyphae levels started high, decreased, and then increased within 20 days, highlighting the dynamic nature of plant-fungal interactions. Overall, our results show that AMF and FRE, not DSE, root colonization rapidly changes over the course of a growing season and these changes are driven by plant phenology and seasonal changes in the environment.

Using Evidence-based Scientific Research to Influence Dietary Behavioral Change: Taking a Look in the Mirror.

Science can provide accurate information to society to inform decision-making and behavior. One contemporary topic in which the science is very clear, yet behavioral change has lagged, is climate change mitigation. Climate change scientists use evidence-based research to advocate to the public to adopt emission-reducing behaviors in various sectors such as transportation and food. However, scientists themselves often do not change their own behaviors according to the scientific consensus. We present a case study of a group of natural sciences PhD students, who, when presented with evidence and an opportunity for a behavioral change with implications for climate change mitigation, demonstrated defensive reactions that would undoubtedly frustrate these same scientists if they were doing public outreach about their own work. Our goal is to raise awareness that we scientists do not always practice what we preach but could perhaps overcome this by understanding the defense mechanisms that impede meaningful change.

Disentangling the effects of sulfate and other seawater ions on microbial communities and greenhouse gas emissions in a coastal forested wetland.

Seawater intrusion into freshwater wetlands causes changes in microbial communities and biogeochemistry, but the exact mechanisms driving these changes remain unclear. Here we use a manipulative laboratory microcosm experiment, combined with DNA sequencing and biogeochemical measurements, to tease apart the effects of sulfate from other seawater ions. We examined changes in microbial taxonomy and function as well as emissions of carbon dioxide, methane, and nitrous oxide in response to changes in ion concentrations. Greenhouse gas emissions and microbial richness and composition were altered by artificial seawater regardless of whether sulfate was present, whereas sulfate alone did not alter emissions or communities. Surprisingly, addition of sulfate alone did not lead to increases in the abundance of sulfate reducing bacteria or sulfur cycling genes. Similarly, genes involved in carbon, nitrogen, and phosphorus cycling responded more strongly to artificial seawater than to sulfate. These results suggest that other ions present in seawater, not sulfate, drive ecological and biogeochemical responses to seawater intrusion and may be drivers of increased methane emissions in soils that received artificial seawater addition. A better understanding of how the different components of salt water alter microbial community composition and function is necessary to forecast the consequences of coastal wetland salinization.

Multiple microbial guilds mediate soil methane cycling along a wetland salinity gradient.

Estuarine wetlands harbor considerable carbon stocks, but rising sea levels could affect their ability to sequester soil carbon as well as their potential to emit methane (CH4). While sulfate loading from seawater intrusion may reduce CH4 production due to the higher energy yield of microbial sulfate reduction, existing studies suggest other factors are likely at play. Our study of 11 wetland complexes spanning a natural salinity and productivity gradient across the San Francisco Bay and Delta found that while CH4 fluxes generally declined with salinity, they were highest in oligohaline wetlands (ca. 3-ppt salinity). Methanogens and methanogenesis genes were weakly correlated with CH4 fluxes but alone did not explain the highest rates observed. Taxonomic and functional gene data suggested that other microbial guilds that influence carbon and nitrogen cycling need to be accounted for to better predict CH4 fluxes at landscape scales. Higher methane production occurring near the freshwater boundary with slight salinization (and sulfate incursion) might result from increased sulfate-reducing fermenter and syntrophic populations, which can produce substrates used by methanogens. Moreover, higher salinities can solubilize ionically bound ammonium abundant in the lower salinity wetland soils examined here, which could inhibit methanotrophs and potentially contribute to greater CH4 fluxes observed in oligohaline sediments.IMPORTANCELow-level salinity intrusion could increase CH4 flux in tidal freshwater wetlands, while higher levels of salinization might instead decrease CH4 fluxes. High CH4 emissions in oligohaline sites are concerning because seawater intrusion will cause tidal freshwater wetlands to become oligohaline. Methanogenesis genes alone did not account for landscape patterns of CH4 fluxes, suggesting mechanisms altering methanogenesis, methanotrophy, nitrogen cycling, and ammonium release, and increasing decomposition and syntrophic bacterial populations could contribute to increases in net CH4 flux at oligohaline salinities. Improved understanding of these influences on net CH4 emissions could improve restoration efforts and accounting of carbon sequestration in estuarine wetlands. More pristine reference sites may have older and more abundant organic matter with higher carbon:nitrogen compared to wetlands impacted by agricultural activity and may present different interactions between salinity and CH4. This distinction might be critical for modeling efforts to scale up biogeochemical process interactions in estuarine wetlands.

Methyl-Based Methanogenesis: an Ecological and Genomic Review.

Methyl-based methanogenesis is one of three broad categories of archaeal anaerobic methanogenesis, including both the methyl dismutation (methylotrophic) pathway and the methyl-reducing (also known as hydrogen-dependent methylotrophic) pathway. Methyl-based methanogenesis is increasingly recognized as an important source of methane in a variety of environments. Here, we provide an overview of methyl-based methanogenesis research, including the conditions under which methyl-based methanogenesis can be a dominant source of methane emissions, experimental methods for distinguishing different pathways of methane production, molecular details of the biochemical pathways involved, and the genes and organisms involved in these processes. We also identify the current gaps in knowledge and present a genomic and metagenomic survey of methyl-based methanogenesis genes, highlighting the diversity of methyl-based methanogens at multiple taxonomic levels and the widespread distribution of known methyl-based methanogenesis genes and families across different environments.

Drivers of bacterial and fungal root endophyte communities: understanding the relative influence of host plant, environment, and space.

Bacterial and fungal root endophytes can impact the fitness of their host plants, but the relative importance of drivers for root endophyte communities is not well known. Host plant species, the composition and density of the surrounding plants, space, and abiotic drivers could significantly affect bacterial and fungal root endophyte communities. We investigated their influence in endophyte communities of alpine plants across a harsh high mountain landscape using high-throughput sequencing. There was less compositional overlap between fungal than bacterial root endophyte communities, with four 'cosmopolitan' bacterial OTUs found in every root sampled, but no fungal OTUs found across all samples. We found that host plant species, which included nine species from three families, explained the greatest variation in root endophyte composition for both bacterial and fungal communities. We detected similar levels of variation explained by plant neighborhood, space, and abiotic drivers on both communities, but the plant neighborhood explained less variation in fungal endophytes than expected. Overall, these findings suggest a more cosmopolitan distribution of bacterial OTUs compared to fungal OTUs, a structuring role of the plant host species for both communities, and largely similar effects of the plant neighborhood, abiotic drivers, and space on both communities.

Methylphosphonate Degradation and Salt-Tolerance Genes of Two Novel Halophilic Marivita Metagenome-Assembled Genomes from Unrestored Solar Salterns.

Aerobic bacteria that degrade methylphosphonates and produce methane as a byproduct have emerged as key players in marine carbon and phosphorus cycles. Here, we present two new draft genome sequences of the genus Marivita that were assembled from metagenomes from hypersaline former industrial salterns and compare them to five other Marivita reference genomes. Phylogenetic analyses suggest that both of these metagenome-assembled genomes (MAGs) represent new species in the genus. Average nucleotide identities to the closest taxon were <85%. The MAGs were assembled with SPAdes, binned with MetaBAT, and curated with scaffold extension and reassembly. Both genomes contained the phnCDEGHIJLMP suite of genes encoding the full C-P lyase pathway of methylphosphonate degradation and were significantly more abundant in two former industrial salterns than in nearby reference and restored wetlands, which have lower salinity levels and lower methane emissions than the salterns. These organisms contain a variety of compatible solute biosynthesis and transporter genes to cope with high salinity levels but harbor only slightly acidic proteomes (mean isoelectric point of 6.48).

Correction: Bueno de Mesquita et al. Methylphosphonate Degradation and Salt-Tolerance Genes of Two Novel Halophilic Marivita Metagenome-Assembled Genomes from Unrestored Solar Salterns. Genes 2022, 13, 148.

The authors have requested that the following change be made to their paper [...].

Dynamic trophic shifts in bacterial and eukaryotic communities during the first 30 years of microbial succession following retreat of an Antarctic glacier.

We examined microbial succession along a glacier forefront in the Antarctic Peninsula representing ∼30 years of deglaciation to contrast bacterial and eukaryotic successional dynamics and abiotic drivers of community assembly using sequencing and soil properties. Microbial communities changed most rapidly early along the chronosequence, and co-occurrence network analysis showed the most complex topology at the earliest stage. Initial microbial communities were dominated by microorganisms derived from the glacial environment, whereas later stages hosted a mixed community of taxa associated with soils. Eukaryotes became increasingly dominated by Cercozoa, particularly Vampyrellidae, indicating a previously unappreciated role for cercozoan predators during early stages of primary succession. Chlorophytes and Charophytes (rather than cyanobacteria) were the dominant primary producers and there was a spatio-temporal sequence in which major groups became abundant succeeding from simple ice Chlorophytes to Ochrophytes and Bryophytes. Time since deglaciation and pH were the main abiotic drivers structuring both bacterial and eukaryotic communities. Determinism was the dominant assembly mechanism for Bacteria, while the balance between stochastic/deterministic processes in eukaryotes varied along the distance from the glacier front. This study provides new insights into the unexpected dynamic changes and interactions across multiple trophic groups during primary succession in a rapidly changing polar ecosystem.

Do plant-soil interactions influence how the microbial community responds to environmental change?

Global change alters ecosystems and their functioning, and biotic interactions can either buffer or amplify such changes. We utilized a long-term nitrogen (N) addition and species removal experiment in the Front Range of Colorado, USA to determine whether a codominant forb and a codominant grass, with different effects on nutrient cycling and plant community structure, would buffer or amplify the effects of simulated N deposition on soil bacterial and fungal communities. While the plant community was strongly shaped by both the presence of dominant species and N addition, we did not find a mediating effect of the plant community on soil microbial response to N. In contrast to our hypothesis, we found a decoupling of the plant and microbial communities such that the soil microbial community shifted under N independently of directional shifts in the plant community. These findings suggest there are not strong cascading effects of N deposition across the plant-soil interface in our system.

Microbial drivers of methane emissions from unrestored industrial salt ponds.

Wetlands are important carbon (C) sinks, yet many have been destroyed and converted to other uses over the past few centuries, including industrial salt making. A renewed focus on wetland ecosystem services (e.g., flood control, and habitat) has resulted in numerous restoration efforts whose effect on microbial communities is largely unexplored. We investigated the impact of restoration on microbial community composition, metabolic functional potential, and methane flux by analyzing sediment cores from two unrestored former industrial salt ponds, a restored former industrial salt pond, and a reference wetland. We observed elevated methane emissions from unrestored salt ponds compared to the restored and reference wetlands, which was positively correlated with salinity and sulfate across all samples. 16S rRNA gene amplicon and shotgun metagenomic data revealed that the restored salt pond harbored communities more phylogenetically and functionally similar to the reference wetland than to unrestored ponds. Archaeal methanogenesis genes were positively correlated with methane flux, as were genes encoding enzymes for bacterial methylphosphonate degradation, suggesting methane is generated both from bacterial methylphosphonate degradation and archaeal methanogenesis in these sites. These observations demonstrate that restoration effectively converted industrial salt pond microbial communities back to compositions more similar to reference wetlands and lowered salinities, sulfate concentrations, and methane emissions.

Methanogenesis and Salt Tolerance Genes of a Novel Halophilic Methanosarcinaceae Metagenome-Assembled Genome from a Former Solar Saltern.

Anaerobic archaeal methanogens are key players in the global carbon cycle due to their role in the final stages of organic matter decomposition in anaerobic environments such as wetland sediments. Here we present the first draft metagenome-assembled genome (MAG) sequence of an unclassified Methanosarcinaceae methanogen phylogenetically placed adjacent to the Methanolobus and Methanomethylovorans genera that appears to be a distinct genus and species. The genome is derived from sediments of a hypersaline (97-148 ppt chloride) unrestored industrial saltern that has been observed to be a significant methane source. The source sediment is more saline than previous sources of Methanolobus and Methanomethylovorans. We propose a new genus name, Methanosalis, to house this genome, which we designate with the strain name SBSPR1A. The MAG was binned with CONCOCT and then improved via scaffold extension and reassembly. The genome contains pathways for methylotrophic methanogenesis from trimethylamine and dimethylamine, as well as genes for the synthesis and transport of compatible solutes. Some genes involved in acetoclastic and hydrogenotrophic methanogenesis are present, but those pathways appear incomplete in the genome. The MAG was more abundant in two former industrial salterns than in a nearby reference wetland and a restored wetland, both of which have much lower salinity levels, as well as significantly lower methane emissions than the salterns.

Structure of Chimpanzee Gut Microbiomes across Tropical Africa.

Understanding variation in host-associated microbial communities is important given the relevance of microbiomes to host physiology and health. Using 560 fecal samples collected from wild chimpanzees (Pan troglodytes) across their range, we assessed how geography, genetics, climate, vegetation, and diet relate to gut microbial community structure (prokaryotes, eukaryotic parasites) at multiple spatial scales. We observed a high degree of regional specificity in the microbiome composition, which was associated with host genetics, available plant foods, and potentially with cultural differences in tool use, which affect diet. Genetic differences drove community composition at large scales, while vegetation and potentially tool use drove within-region differences, likely due to their influence on diet. Unlike industrialized human populations in the United States, where regional differences in the gut microbiome are undetectable, chimpanzee gut microbiomes are far more variable across space, suggesting that technological developments have decoupled humans from their local environments, obscuring regional differences that could have been important during human evolution. IMPORTANCE Gut microbial communities are drivers of primate physiology and health, but the factors that influence the gut microbiome in wild primate populations remain largely undetermined. We report data from a continent-wide survey of wild chimpanzee gut microbiota and highlight the effects of genetics, vegetation, and potentially even tool use at different spatial scales on the chimpanzee gut microbiome, including bacteria, archaea, and eukaryotic parasites. Microbial community dissimilarity was strongly correlated with chimpanzee population genetic dissimilarity, and vegetation composition and consumption of algae, honey, nuts, and termites were potentially associated with additional divergence in microbial communities between sampling sites. Our results suggest that host genetics, geography, and climate play a far stronger role in structuring the gut microbiome in chimpanzees than in humans.

Limited Response of Indigenous Microbes to Water and Nutrient Pulses in High-Elevation Atacama Soils: Implications for the Cold-Dry Limits of Life on Earth.

Soils on the world's highest volcanoes in the Atacama region represent some of the harshest ecosystems yet discovered on Earth. Life in these environments must cope with high UV flux, extreme diurnal freeze-thaw cycles, low atmospheric pressure and extremely low nutrient and water availability. Only a limited spectrum of bacterial and fungal lineages seems to have overcome the harshness of this environment and may have evolved the ability to function in situ. However, these communities may lay dormant for most of the time and spring to life only when enough water and nutrients become available during occasional snowfalls and aeolian depositions. We applied water and nutrients to high-elevation soils (5100 meters above sea level) from Volcán Llullaillaco, both in lab microcosms and in the field, to investigate how microbial communities respond when resource limitations are alleviated. The dominant taxon in these soils, the extremophilic yeast Naganishia sp., increased in relative sequence abundance and colony-forming unit counts after water + nutrient additions in microcosms, and marginally in the field after only 6 days. Among bacteria, only a Noviherbaspirillum sp. (Oxalobacteraceae) significantly increased in relative abundance both in the lab and field in response to water addition but not in response to water and nutrients together, indicating that it might be an oligotroph uniquely suited to this extreme environment. The community structure of both bacteria and eukaryotes changed significantly with water and water + nutrient additions in the microcosms and taxonomic richness declined with amendments to water and nutrients. These results indicate that only a fraction of the detected community is able to become active when water and nutrients limitations are alleviated in lab microcosms, and that water alone can dramatically change community structure. Our study sheds light on which extremophilic organisms are likely to respond when favorable conditions occur in extreme earthly environments and perhaps in extraterrestrial environments as well.

Growing-season length and soil microbes influence the performance of a generalist bunchgrass beyond its current range.

As organisms shift their geographic distributions in response to climate change, biotic interactions have emerged as an important factor driving the rate and success of range expansions. Plant-microbe interactions are an understudied but potentially important factor governing plant range shifts. We studied the distribution and function of microbes present in high-elevation unvegetated soils, areas that plants are colonizing as climate warms, snow melts earlier, and the summer growing season lengthens. Using a manipulative snowpack and microbial inoculation transplant experiment, we tested the hypothesis that growing-season length and microbial community composition interact to control plant elevational range shifts. We predicted that a lengthening growing season combined with dispersal to patches of soils with more mutualistic microbes and fewer pathogenic microbes would facilitate plant survival and growth in previously unvegetated areas. We identified negative effects on survival of the common alpine bunchgrass Deschampsia cespitosa in both short and long growing seasons, suggesting an optimal growing-season length for plant survival in this system that balances time for growth with soil moisture levels. Importantly, growing-season length and microbes interacted to affect plant survival and growth, such that microbial community composition increased in importance in suboptimal growing-season lengths. Further, plants grown with microbes from unvegetated soils grew as well or better than plants grown with microbes from vegetated soils. These results suggest that the rate and spatial extent of plant colonization of unvegetated soils in mountainous areas experiencing climate change could depend on both growing-season length and soil microbial community composition, with microbes potentially playing more important roles as growing seasons lengthen.

Soil Microbial Networks Shift Across a High-Elevation Successional Gradient.

While it is well established that microbial composition and diversity shift along environmental gradients, how interactions among microbes change is poorly understood. Here, we tested how community structure and species interactions among diverse groups of soil microbes (bacteria, fungi, non-fungal eukaryotes) change across a fundamental ecological gradient, succession. Our study system is a high-elevation alpine ecosystem that exhibits variability in successional stage due to topography and harsh environmental conditions. We used hierarchical Bayesian joint distribution modeling to remove the influence of environmental covariates on species distributions and generated interaction networks using the residual species-to-species variance-covariance matrix. We hypothesized that as ecological succession proceeds, diversity will increase, species composition will change, and soil microbial networks will become more complex. As expected, we found that diversity of most taxonomic groups increased over succession, and species composition changed considerably. Interestingly, and contrary to our hypothesis, interaction networks became less complex over succession (fewer interactions per taxon). Interactions between photosynthetic microbes and any other organism became less frequent over the gradient, whereas interactions between plants or soil microfauna and any other organism were more abundant in late succession. Results demonstrate that patterns in diversity and composition do not necessarily relate to patterns in network complexity and suggest that network analyses provide new insight into the ecology of highly diverse, microscopic communities.