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Kostka, J. E.

Publications and source records attributed to Kostka, J. E..

14 recordsLinked to original sources

Leaf Damage Is Associated with Microbiome Dysbiosis in the Spartina alterniflora Phyllosphere

Spartina alterniflora, the dominant plant species in salt marshes along the Atlantic and Gulf of Mexico coastlines of the Americas, is affected by disease and sudden vegetation dieback. Despite the foundational role of S. alterniflora in low-elevation salt marshes, the response of the native leaf-associated microbiome (i.e., phyllosphere microbiome) to leaf damage resulting from disease and environmental stress has not been explored. We hypothesized that healthy and damaged plants would show differentiation in their phyllosphere microbiomes following primary infection or exposure to environmental stressors. Here, we analyzed changes in prokaryotic and fungal relative abundance, diversity, and community composition in the S. alterniflora phyllosphere microbiome. We compared natural marsh and greenhouse plants in Georgia and South Carolina, USA, and collected leaves from healthy and damaged natural plants across two contrasting Spartina phenotypes that differ in their exposure to environmental stress. Our results show that plant origin (i.e., greenhouse vs. natural marsh), plant health status (i.e., healthy vs. damaged), and plant phenotype (i.e., short vs. tall Spartina) affect microbial relative abundance, alpha diversity, and community composition in the S. alterniflora phyllosphere. Damaged leaves presented higher microbial abundance and alpha diversity than healthy leaves, suggesting microbial proliferation following leaf damage. Plants raised from seeds in the greenhouse presented the lowest microbial abundance and Shannon diversity for both prokaryotic and fungal communities, indicating that in natural ecosystems the phyllosphere microbiota is acquired predominantly through horizontal transmission from the environment. Overall, this study provides novel insights into the assembly of the S. alterniflora phyllosphere microbiome. ImportanceSalt marshes are tidally influenced coastal wetlands that provide a range of ecosystem services to global and local communities, including protection from storm surge, water purification, and carbon sequestration. Spartina alterniflora is the dominant plant species in Atlantic and Gulf of Mexico marshes in the Americas. Fungal disease and exposure to environmental stressors have previously been described in marsh ecosystems and linked to extensive and sudden vegetation dieback in the southeastern U.S. In this study, we propose that microbial proliferation follows plant damage caused by either fungal disease or environmental stress, leading to profound changes in native leaf-associated microbiota abundance, diversity, and composition. Using greenhouse plants as a control, we also demonstrate that microbes colonizing marsh leaves are acquired predominantly from the environment. Overall, this study advances the ecological understanding of the S. alterniflora leaf microbiome assembly, establishing a baseline to inform future work harnessing plant-associated microbes for ecosystem restoration.

microbiology↗

Viral community diversity in the rhizosphere of the foundation salt marsh plant Spartina alterniflora

Viruses of microorganisms impact microbial population dynamics, community structure, nutrient cycling, gene transfer, and genomic innovation. In wetlands, root-associated microbial communities mediate key biogeochemical processes important for plants involved in ecosystem maintenance. Nonetheless, the presence and role of microbial viruses in salt marshes remains poorly understood. In this study, we analyzed 24 metagenomes retrieved from the root zone of Spartina alterniflora, a foundation plant in salt marshes of the eastern and Gulf coasts of the U.S. The samples span three plant compartments--bulk sediment, rhizosphere, and root--and two cordgrass plant phenotypes: short and tall. We observed differentiation between phenotypes and increased similarity in viral communities between the root and rhizosphere, indicating that plant compartment and phenotype shape viral community composition. The majority of viral populations characterized are novel at the genus level, with a subset predicted to target microorganisms known to carry out key biogeochemical functions. The findings provide a holistic assessment of plant-associated viral diversity and community composition as well as identifying potential targets for exploring viral modulation of microbially-mediated ecosystem functioning in intertidal wetlands. ImportanceSalt marshes are vital coastal ecosystems. Microbes in these environments drive nutrient cycling and support plant health, with Spartina alterniflora serving as a foundation species. This study explores viral communities associated with S. alterniflora, revealing how plant compartment and phenotype shape viral composition. The discovery of numerous novel viruses, some potentially influencing microbes involved in key biogeochemical processes, highlights their ecological significance. Given the increasing pressures on coastal ecosystems, understanding virus-microbe-plant interactions is essential for predicting and managing ecosystem responses to environmental change.

genomics↗

Northern peatland microbial networks exhibit resilience to warming and acquire electron acceptor from soil organic matter

The microbial networks that regulate belowground carbon turnover and respond to climate change drivers in peatlands are poorly understood. Here, we leverage a whole ecosystem warming experiment to elucidate the key processes of terminal carbon decomposition and community responses to temperature rise. Our dataset of 697 metagenome-assembled genomes (MAGs) extends from surface (10 cm) to 2 m deep into the peat column, with only 3.7% of genomes overlapping with other well-studied peatlands. Unexpectedly, community composition has yet to show a significant response to warming after 3 years, suggesting that metabolically diverse soil microbial networks are resilient to climate change. Surprisingly, the dominant methanogens showed the potential for both acetoclastic and hydrogenotrophic methanogenesis. Nonetheless, the predominant pathways for anaerobic carbon decomposition include sulfate/sulfite reduction, denitrification, and acetogenesis, rather than methanogenesis based on gene abundances. Multi-omics data suggest that organic matter cleavage provides terminal electron acceptors, whichtogether with methanogen metabolic flexibility, may explain peat microbiome resilience to warming.

microbiology↗

Metabolic interactions underpinning high methane fluxes across terrestrial freshwater wetlands

Current estimates of wetland contributions to the global methane budget carry high uncertainty, particularly in accurately predicting emissions from high methane-emitting wetlands. Microorganisms mediate methane cycling, yet knowledge of their conservation across wetlands remains scarce. To address this, we integrated 1,118 16S rRNA amplicon datasets (116 new), 305 metagenomes (20 new) that yielded 4,745 medium and high-quality metagenome assembled genomes (MAGs; 617 new), 133 metatranscriptomes, and annual methane flux data across 9 wetlands to create the Multi-Omics for Understanding Climate Change (MUCC) v2.0.0 database. This new resource was leveraged to link microbiome compositional profiles to encoded functions and emissions, with specific focus on methane-cycling populations and the microbial carbon decomposition networks that fuel them. We identified eight methane-cycling genera that were conserved across wetlands, and deciphered wetland specific metabolic interactions across marshes, revealing low methanogen-methanotroph connectivity in high-emitting wetlands. Methanoregula emerged as a hub methanogen across networks and was a strong predictor of methane flux, demonstrating the potential broad relevance of methylotrophic methanogenesis in these ecosystems. Collectively, our findings illuminate trends between microbial decomposition networks and methane flux and provide an extensive publicly available database to advance future wetland research.

microbiology↗

Sulfur oxidation and reduction are coupled to nitrogen fixation in the roots of a salt marsh foundation plant species

Symbiotic root microbiota are crucial for plant growth as they assist their hosts in nutrient acquisition. In the roots of coastal marine plants, heterotrophic activity in the rhizosphere by sulfate-reducing microorganisms has been linked to nitrogen fixation. In this study, we recovered 239 high-quality metagenome-assembled genomes (MAGs) from a salt marsh dominated by the foundation plant Spartina alterniflora, including diazotrophic sulfate-reducing and sulfur-oxidizing bacteria thriving in the root compartment. Here we show for the first time that highly-abundant sulfur-oxidizing bacteria in the roots of a coastal macrophyte encode and highly express genes for nitrogen fixation (nifHDK). Further, we leveraged a S. alterniflora biomass gradient to gain a mechanistic understanding on how root-microbe interactions respond to abiotic stress from anoxia and elevated sulfide concentration. We observed that the roots of the stressed S. alterniflora phenotype exhibited the highest rates of nitrogen fixation and expression levels of both the oxidative and reductive forms of the dissimilatory sulfite reductase gene (dsrAB). Approximately 25% and 15% of all sulfur-oxidizing dsrA and nitrogen-fixing nifK transcripts, respectively, were associated with novel MAGs of the Candidatus Thiodiazotropha genus in the roots of the stressed S. alterniflora phenotype. We conclude that the rapid cycling of sulfur in the dynamic S. alterniflora root zone is coupled to nitrogen fixation during both reductive and oxidative sulfur reactions, and that the S. alterniflora - Ca. Thiodiazotropha symbiosis is an adaptive response to anoxic and sulfidic sediment conditions, whereby the plants benefit from reduced sulfide toxicity and potential nitrogen acquisition.

microbiology↗

Severe drought events trigger long-term salt marsh dieback in the Southeastern and Gulf of Mexico USA

The frequency of salt marsh dieback events has increased over the last 25 years with unknown consequences to the resilience of the ecosystem to accelerated sea level rise (SLR). Salt marsh ecosystems impacted by sudden vegetation dieback events were previously thought to recover naturally within a few months to years. In this study, we provide evidence that approximately 14% of total marsh area has not revegetated 10-years after a dieback event in Charleston, SC. Dieback onset coincided with a severe drought in 2012, and a second dieback event occurred in 2016 after a historic flood influenced by Hurricane Joaquin in October of 2015, with unvegetated zones reaching nearly 30% of total marsh area in 2017. Most affected areas were associated with lower elevation zones in the interior of the marsh (midmarsh). During the 2013 dieback event, we estimate that unvegetated midmarsh area expanded by 300%. Grass planting was shown to be an effective restoration practice, with restored plants having greater aboveground biomass than relict sites after two years of transplanting. A positive restoration outcome indicated that the stressors that caused the initial dieback are no longer present. Despite that, many dieback areas have not recovered naturally even as they are located within the typical elevation range of a healthy vegetated marsh. A mechanistic modelling approach was used to assess the effects of vegetation dieback on salt marsh resilience to SLR. Predictions indicate that a highly productive restored marsh (2000 g m-2 y-1) would persist at a moderate SLR rate of 60 cm 100 y-1, whereas a non- restored mudflat would lose all of its elevation capital after 100 years. Thus, rapid restoration of marsh dieback is critical to avoid further degradation. Also, failure to incorporate the increasing frequency and intensity of extreme climatic events which trigger irreversible marsh diebacks underestimates salt marsh vulnerability to climate change. At an elevated SLR rate of 122 cm 100 y-1, most likely an extreme climate change scenario, even highly productive ecosystems augmented by sediment placement would not keep pace with SLR. Thus, climate change mitigation actions are also urgently needed to preserve present-day marsh ecosystems.

ecology↗

The core root microbiome of Spartina alterniflora is predominated by sulfur-oxidizing and sulfate-reducing bacteria in Georgia salt marshes, USA

BackgroundSalt marshes are dominated by the smooth cordgrass Spartina alterniflora on the US Atlantic and Gulf of Mexico coastlines. Although soil microorganisms are well known to mediate important biogeochemical cycles in salt marshes, little is known about the role of root microbiomes in supporting the health and productivity of marsh plant hosts. Leveraging in situ gradients in aboveground plant biomass as a natural laboratory, we investigated the relationships between S. alterniflora primary productivity, sediment redox potential, and the physiological ecology of bulk sediment, rhizosphere, and root microbial communities at two Georgia barrier islands over two growing seasons. ResultsA marked decrease in prokaryotic alpha diversity with high abundance and increased phylogenetic dispersion was found in the S. alterniflora root microbiome. Significantly higher rates of enzymatic organic matter decomposition, as well as the relative abundances of putative sulfur (S)-oxidizing, sulfate-reducing, and nitrifying prokaryotes correlated with plant productivity. Moreover, these functional guilds were overrepresented in the S. alterniflora rhizosphere and root core microbiomes. Core microbiome bacteria from the Candidatus Thiodiazotropha genus, with the metabolic potential to couple S oxidation with C and N fixation, were shown to be highly abundant in the root and rhizosphere of S. alterniflora. ConclusionsThe S. alterniflora root microbiome is dominated by highly active and competitive species taking advantage of available carbon substrates in the oxidized root zone. Two microbially-mediated mechanisms are proposed to stimulate S. alterniflora primary productivity: (i.) Enhanced microbial activity replenishes nutrients and terminal electron acceptors in higher biomass stands, and (ii.) coupling of chemolithotrophic S oxidation with carbon (C) and nitrogen (N) fixation by root and rhizosphere associated prokaryotes detoxify sulfide in the root zone while potentially transferring fixed C and N to the host plant.

microbiology↗

Minnesota peat viromes reveal terrestrial and aquatic niche partitioning for local and global viral populations

BackgroundPeatlands are expected to experience sustained yet fluctuating higher temperatures due to climate change, leading to increased microbial activity and greenhouse gas emissions. Despite mounting evidence for viral contributions to these processes in peatlands underlain with permafrost, little is known about viruses in other peatlands. More generally, soil viral biogeography and its potential drivers are poorly understood at both local and global scales. Here, 87 metagenomes and five viral size-fraction metagenomes (viromes) from a boreal peatland in northern Minnesota (the SPRUCE whole-ecosystem warming experiment and surrounding bog) were analyzed for dsDNA viral community ecological patterns, and the recovered viral populations (vOTUs) were compared to our curated PIGEON database of 266,805 vOTUs from diverse ecosystems. ResultsWithin the SPRUCE experiment, viral community composition was significantly correlated with peat depth, water content, and carbon chemistry, including CH4 and CO2 concentrations, but not with temperature during the first two years of warming treatments. Peat vOTUs with aquatic-like signatures (shared predicted protein content with marine and/or freshwater vOTUs) were significantly enriched in more waterlogged surface peat depths. Predicted host ranges for SPRUCE vOTUs were relatively narrow, generally within a single bacterial genus. Of the 4,326 SPRUCE vOTUs, 164 were previously detected in other soils, mostly peatlands. None of the previously identified 202,372 marine and freshwater vOTUs in our PIGEON database were detected in SPRUCE peat, but 1.9% of 78,203 genus-level viral clusters (VCs) were shared between soil and aquatic environments. On a per-sample basis, vOTU recovery was 32 times higher from viromes compared to total metagenomes. ConclusionsResults suggest strong viral "species" boundaries between terrestrial and aquatic ecosystems and to some extent between peat and other soils, with differences less pronounced at the "genus" level. The significant enrichment of aquatic-like vOTUs in more waterlogged peat suggests that viruses may also exhibit niche partitioning on more local scales. These patterns are presumably driven in part by host ecology, consistent with the predicted narrow host ranges. Although more samples and increased sequencing depth improved vOTU recovery from total metagenomes, the substantially higher per-sample vOTU recovery after viral particle enrichment highlights the utility of soil viromics.

microbiology↗

Genome Repository of Oiled Systems (GROS): an interactive and searchable database that expands the catalogued diversity of crude oil-associated microbes

Indigenous microbial communities ultimately control the fate of petroleum hydrocarbons (PHCs) that enters the natural environment through natural seeps or accidental oil spills, but the interactions among microbes and with their chemical environment during oil biodegradation are highly complex and poorly understood. Genome-resolved metagenomics have the potential to help in unraveling these complex interactions. However, the lack of a comprehensive database that integrates existing genomic/metagenomic data from oiled environments with physicochemical parameters known to regulate the fate of PHCs currently limits data analysis and interpretations. Here, we present a curated, comprehensive, and searchable database that documents microbial populations in oiled ecosystems on a global scale, along with underlying physicochemical data, geocoded via GIS to reveal geographic distribution patterns of the populations. Analysis of the ~2,000 metagenome-assembled genomes (MAGs) available in the database revealed strong ecological niche specialization within habitats e.g., specialization to coastal sediments vs. water-column vs. deep-sea sediments. Over 95% of the recovered MAGs represented novel and uncultured species underscoring the limited representation of cultured organisms from oil-contaminated and oil reservoir ecosystems. The majority of MAGs linked to oiled ecosystems are members of the rare biosphere in non-oiled samples, except for the Gulf of Mexico (GoM) which appears to be primed for oil biodegradation. GROS should facilitate future work toward a more predictive understanding of the microbial taxa and their activities that control the fate of oil spills as well as serve as a model approach for building similar resources for additional environmental processes and omic data of interest.

genomics↗

Genomic characterization and computational phenotyping of nitrogen-fixing bacteria isolated from Colombian sugarcane fields

Previous studies have shown that the sugarcane microbiome harbors diverse plant growth promoting (PGP) microorganisms, including nitrogen-fixing bacteria, and the objective of this study was to design a genome-enabled approach to prioritize sugarcane associated nitrogen-fixing bacteria according to their potential as biofertilizers. Using a systematic high throughput approach, 22 pure cultures of nitrogen-fixing bacteria were isolated and tested for diazotrophic potential by PCR amplification of nitrogenase (nifH) genes, common molecular markers for nitrogen fixation capacity. Genome sequencing confirmed the presence of intact nitrogenase nifH genes and operons in the genomes of 18 of the isolates. Isolate genomes also encoded operons for phosphate solubilization, siderophore production operons, and other PGP phenotypes. Klebsiella pneumoniae strains comprised 14 of the 22 nitrogen-fixing isolates, and four others were members of closely related genera to Klebsiella. A computational phenotyping approach was developed to rapidly screen for strains that have high potential for nitrogen fixation and other PGP phenotypes while showing low risk for virulence and antibiotic resistance. The majority of sugarcane isolates were below a genotypic and phenotypic threshold, showing uniformly low predicted virulence and antibiotic resistance compared to clinical isolates. Six prioritized strains were experimentally evaluated for PGP phenotypes: nitrogen fixation, phosphate solubilization, and the production of siderophores, gibberellic acid and indole acetic acid. Results from the biochemical assays were consistent with the computational phenotype predictions for these isolates. Our results indicate that computational phenotyping is a promising tool for the assessment of benefits and risks associated with bacteria commonly detected in agricultural ecosystems.\n\nIMPORTANCEA genome-enabled approach was developed for the prioritization of native bacterial isolates with the potential to serve as biofertilizers for sugarcane fields in Colombias Cauca Valley. The approach is based on computational phenotyping, which entails predictions related to traits of interest based on bioinformatic analysis of whole genome sequences. Bioinformatic predictions of the presence of plant growth promoting traits were validated with experimental assays and more extensive genome comparisons, thereby demonstrating the utility of computational phenotyping for assessing the benefits and risks posed by bacterial isolates that can be used as biofertilizers. The quantitative approach to computational phenotyping developed here for the discovery of biofertilizers has the potential for use with a broad range of applications in environmental and industrial microbiology, food safety, water quality, and antibiotic resistance studies.

microbiology↗

Defining the seafloor microbiome of the Gulf of Mexico and its response to oil perturbation

The microbial ecology of oligotrophic deep ocean sediments is understudied relative to their shallow counterparts, and this lack of understanding hampers our ability to predict responses to current and future perturbations. The Gulf of Mexico has experienced two of the largest accidental marine oil spills, the 1979 Ixtoc-1 blowout and the 2010 Deepwater Horizon (DWH) discharge. Here, microbial communities were characterized for 29 sites across multiple years in >700 samples. The composition of the seafloor microbiome was broadly consistent across the region and was well approximated by the overlying water depth and depth within the sediment column, while geographic distance played a limited role. Biogeographical distributions were employed to generate predictive models for over 4000 OTU that leverage easy-to-obtain geospatial variables which are linked to measured sedimentary oxygen profiles. Depth stratification and putative niche diversification are evidenced by the distribution of taxa that mediate the microbial nitrogen cycle. Further, these results demonstrate that sediments impacted by the DWH spill had returned to near baseline conditions after two years. The distributions of benthic microorganisms in the Gulf can be constrained, and moreover deviations from these predictions may pinpoint impacted sites and aid in future response efforts or long-term stability studies.

ecology↗

Diversity of active viral infections within the Sphagnum microbiome

Sphagnum-dominated peatlands play an important role in global carbon storage and represent significant sources of economic and ecological value. While recent efforts to describe microbial diversity and metabolic potential of the Sphagnum microbiome have demonstrated the importance of its microbial community, little is known about the viral constituents. We used metatranscriptomics to describe the diversity and activity of viruses infecting microbes within the Sphagnum peat bog. The vegetative portions of 6 Sphagnum plants were obtained from a peatland in northern Minnesota and total RNA extracted and sequenced. Metatranscriptomes were assembled and contigs screened for the presence of conserved virus marker genes. Using bacteriophage capsid protein, gp23, as a marker for phage diversity, we identified 33 contigs representing undocumented phage s that were active in the community at the time of sampling. Similarly, RNA-dependent RNA polymerase and the Nucleo-Cytoplasmic Large DNA Virus (NCLDV) major capsid protein were used as markers for ssRNA viruses and NCLDV, respectively. In total 114 contigs were identified as originating from undescribed ssRNA viruses, 22 of which represent near-complete genomes. An additional 64 contigs were identified as being from NCLDVs. Finally, 7 contigs were identified as putative virophage or polinto-like viruses. We developed co-occurrence networks with these markers in relation to the expression of potential-host housekeeping gene rpb1 to predict virus-host relationships, identifying 13 groups. Together, our approach offers new tools for the identification of virus diversity and interactions in understudied clades, and suggest viruses may play a considerable role in the ecology of the Sphagnum microbiome.\n\nSignificanceSphagnum-dominated peatlands play an important role in maintaining atmospheric carbon dioxide levels by modifying conditions in the surrounding soil to favor its own growth over other plant species. This slows rates of decomposition and facilitates the accumulation of fixed carbon in the form of partially decomposed biomass. The unique environment produced by Sphagnum enriches for the growth of a diverse microbial consortia that benefit from and support the mosss growth, while also maintaining the hostile soil conditions. While a growing body of research has begun to characterize the microbial groups that colonize Sphagnum, little is currently known about the ecological factors that constrain community structure and define ecosystem function. Top-down population control by viruses is almost completely undescribed. This study provides insight into the significant viral influence on the Sphagnum microbiome, and identifying new potential model systems to study virus-host interactions in the peatland ecosystem.

microbiology↗

Experimental warming reduces the diversity and functional potential of the Sphagnum microbiome

Climate change may reduce biodiversity leading to a reduction in ecosystem productivity. Despite numerous reports of a strong correlation of microbial diversity and ecosystem productivity, little is known about the warming effects on plant associated microbes. Here we explore the impact of experimental warming on the microbial and nitrogen-fixing (diazotroph) community associated with the widespread and ecologically relevant Sphagnum genus in a field warming experiment. To quantify changes in the abundance, diversity, and community composition of Sphagnum microbiomes with warming we utilized qPCR and Illumina sequencing of the 16S SSU rRNA and nifH gene. Microbial and diazotroph community richness and Shannon diversity decreased with warming (p<0.05). The diazotroph communities shifted from diverse communities to domination by primarily Nostocaceae (25% in control samples to 99% in elevated temperature samples). In addition, the nitrogen fixation activity measured with the acetylene reduction assay (ARA) decreased with warming treatment. This suggests the negative correlation of temperature and microbial diversity corresponds to a reduction in functional potential within the diazotroph community. The results indicate that climate warming may alter the community structure and function in peat moss microbiomes, with implications for impacts to host fitness and ecosystem productivity, and carbon uptake potential of peatlands.

ecology↗

Alphaproteobacteria fix nitrogen in a Sphagnum-dominated peat bog using molybdenum-dependent nitrogenase

Microbial N2 fixation (diazotrophy) represents an important nitrogen source to oligotrophic peatland ecosystems, which are important sinks for atmospheric CO2 and susceptible to changing climate. The objectives of this study were: (i) to determine the active microbial group and type of nitrogenase mediating diazotrophy in a ombrotrophic Sphagnum-dominated peat bog (the S1 peat bog, Marcell Experimental Forest, Minnesota, USA); and (ii) to determine the effect of environmental parameters (light, O2, CO2, CH4) on potential rates of diazotrophy measured by acetylene (C2H2) reduction and 15N2 incorporation. Molecular analysis of metabolically active microbial communities suggested that diazotrophy in surface peat was primarily mediated by Alphaproteobacteria (Bradyrhizobiaceae and Beijerinckiaceae). Despite higher dissolved vanadium (V; 11 nM) than molybdenum (Mo; 3 nM) in surface peat, a combination of metagenomic, amplicon sequencing and activity measurements indicated that Mo-containing nitrogenases dominate over the V-containing form. Acetylene reduction was only detected in surface peat exposed to light, with the highest rates observed in peat collected from hollows with the highest water content. Incorporation of15N2 was suppressed 90% by O2 and 55% by C2H2, and was unaffected by CH4 and CO2 amendments. These results suggest that peatland diazotrophy is mediated by a combination of C2H2 - sensitive and C2H2 - insensitive microbes that are more active at low O2 and show similar activity at high and low CH4.\n\nImportancePrevious studies indicate that diazotrophy provides an important nitrogen source and is linked to methanotrophy in Sphagnum-dominated peatlands. However, the environmental controls and enzymatic pathways of peatland diazotrophy, as well as the metabolically active microbial populations that catalyze this process remain in question. Our findings indicate that oxygen levels and photosynthetic activity override low nutrient availability in limiting diazotrophy, and that members of the Alphaproteobacteria (Rhizobiales) catalyze this process at the bog surface using the molybdenum - based form of the nitrogenase enzyme.

microbiology↗