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Climate warming in the Arctic is thawing previously frozen soil (permafrost). Permafrost thaw alters landscape hydrology and increases weathering rates, which can increase the delivery of solutes to adjacent waters. Long-term river monitoring of the Kuparuk River (North Slope, Alaska, USA) confirms significant increases in solutes that are indicative of thawing permafrost. However, there is no evidence of an increase in total phosphorus (TP) or soluble reactive phosphorus (SRP), the nutrient that limits primary production in this and similar rivers in the region. Here, we show that Mehlich-3 extractable iron (Fe) and aluminum (Al) impart high P biogeochemical sorption capacities across a range of landscape features that we would expect to promote lateral movement of water and solutes to headwater streams in our study watershed. Reanalysis of a recently published pan-Arctic soils database suggests that this high P sorption capacity could be common in other parts of the Arctic region. We conclude that while warming-induced permafrost thaw may increase the potential for P mobility in our watershed, simultaneous increases in pedogenic secondary Fe and Al minerals may continue to retain P in these soils and limit biological productivity in the adjacent river. We suggest that similar interactions may occur in other areas of the Arctic where comparable biogeochemical conditions prevail. 

ABSTRACT Leptothrix ochracea creates distinctive iron-mineralized mats that carpet streams and wetlands. Easily recognized by its iron-mineralized sheaths, L. ochracea was one of the first microorganisms described in the 1800s. Yet it has never been isolated and does not have a complete genome sequence available, so key questions about its physiology remain unresolved. It is debated whether iron oxidation can be used for energy or growth and if L. ochracea is an autotroph, heterotroph, or mixotroph. To address these issues, we sampled L. ochracea-rich mats from three of its typical environments (a stream, wetlands, and a drainage channel) and reconstructed nine high-quality genomes of L. ochracea from metagenomes. These genomes contain iron oxidase genes cyc2 andmtoA, showing that L. ochracea has the potential to conserve energy from iron oxidation. Sox genes confer potential to oxidize sulfur for energy. There are genes for both carbon fixation (RuBisCO) and utilization of sugars and organic acids (acetate, lactate, and formate). In silico stoichiometric metabolic models further demonstrated the potential for growth using sugars and organic acids. Metatranscriptomes showed a high expression of genes for iron oxidation; aerobic respiration; and utilization of lactate, acetate, and sugars, as well as RuBisCO, supporting mixotrophic growth in the environment. In summary, our results suggest that L. ochracea has substantial metabolic flexibility. It is adapted to iron-rich, organic carbon-containing wetland niches, where it can thrive as a mixotrophic iron oxidizer by utilizing both iron oxidation and organics for energy generation and both inorganic and organic carbon for cell and sheath production. IMPORTANCEWinogradsky's observations of L. ochracea led him to propose autotrophic iron oxidation as a new microbial metabolism, following his work on autotrophic sulfur-oxidizers. While much culture-based research has ensued, isolation proved elusive, so most work on L. ochracea has been based in the environment and in microcosms. Meanwhile, the autotrophic Gallionella became the model for freshwater microbial iron oxidation, while heterotrophic and mixotrophic iron oxidation is not well-studied. Ecological studies have shown that Leptothrix overtakes Gallionella when dissolved organic carbon content increases, demonstrating distinct niches. This study presents the first near-complete genomes of L. ochracea, which share some features with autotrophic iron oxidizers, while also incorporating heterotrophic metabolisms. These genome, metabolic modeling, and transcriptome results give us a detailed metabolic picture of how the organism may combine lithoautotrophy with organoheterotrophy to promote Fe oxidation and C cycling and drive many biogeochemical processes resulting from microbial growth and iron oxyhydroxide formation in wetlands. 

Abstract Water logged habitats in continuous permafrost regions provide extensive oxic-anoxic interface habitats for iron cycling. The iron cycle interacts with the methane and phosphorus cycles, and is an important part of tundra biogeochemistry. Our objective was to characterize microbial communities associated with the iron cycle within natural and disturbed habitats of the Alaskan Arctic tundra. We sampled aquatic habitats within natural, undisturbed and anthropogenically disturbed areas and sequenced the 16S rRNA gene to describe the microbial communities, then supported these results with process rate and geochemical measurements. Undisturbed habitats have microbial communities that are significantly different than disturbed habitats. Microbial taxa known to participate in the iron and methane cycles are significantly associated with natural habitats, whereas they are not significantly associated with disturbed sites. Undisturbed habitats have significantly higher extractable iron and are more acidic than disturbed habitats sampled. Iron reduction is not measurable in disturbed aquatic habitats and is not stimulated by the addition of biogenic iron mats. Our study highlights the prevalence of Fe-cycling in undisturbed water-logged habitats, and demonstrates that anthropogenic disturbance of the tundra, due to legacy gravel mining, alters the microbiology of aquatic habitats and disrupts important biogeochemical cycles in the Arctic tundra. 

Rates of microbial processes are fundamental to understanding the significance of microbial impacts on environmental chemical cycling. However, it is often difficult to quantify rates or to link processes to specific taxa or individual cells, especially in environments where there are few cultured representatives with known physiology. Here, we describe the use of the redox-enzyme-sensitive molecular probe RedoxSensor™ Green to measure rates of anaerobic electron transfer physiology (i.e., sulfate reduction and methanogenesis) in individual cells and link those measurements to genomic sequencing of the same single cells. We used this method to investigate microbial activity in hot, anoxic, low-biomass (~10³cells mL⁻¹) groundwater of the Death Valley Regional Flow System, California. Combining this method with electron donor amendment experiments and metatranscriptomics confirmed that the abundant spore formers includingCandidatusDesulforudis audaxviator were actively reducing sulfate in this environment, most likely with acetate and hydrogen as electron donors. Using this approach, we measured environmental sulfate reduction rates at 0.14 to 26.9 fmol cell⁻¹h⁻¹. Scaled to volume, this equates to a bulk environmental rate of ~10³pmol sulfate L⁻¹d⁻¹, similar to potential rates determined with radiotracer methods. Despite methane in the system, there was no evidence for active microbial methanogenesis at the time of sampling. Overall, this method is a powerful tool for estimating species-resolved, single-cell rates of anaerobic metabolism in low-biomass environments while simultaneously linking genomes to phenomes at the single-cell level. We reveal active elemental cycling conducted by several species, with a large portion attributable toCa.Desulforudis audaxviator. 

Redox active species in Arctic lacustrine sediments play an important, regulatory role in the carbon cycle, yet there is little information on their spatial distribution, abundance, and oxidation states. Here, we use voltammetric microelectrodes to quantify the in situ concentrations of redox-active species at high vertical resolution (mm to cm) in the benthic porewaters of an oligotrophic Arctic lake (Toolik Lake, AK, USA). Mn( ii ), Fe( ii ), O 2 , and Fe( iii )-organic complexes were detected as the major redox-active species in these porewaters, indicating both Fe( ii ) oxidation and reductive dissolution of Fe( iii ) and Mn( iv ) minerals. We observed significant spatial heterogeneity in their abundance and distribution as a function of both location within the lake and depth. Microbiological analyses and solid phase Fe( iii ) measurements were performed in one of the Toolik Lake cores to determine the relationship between biogeochemical redox gradients and microbial communities. Our data reveal iron cycling involving both oxidizing (FeOB) and reducing (FeRB) bacteria. Additionally, we profiled a large microbial iron mat in a tundra seep adjacent to an Arctic stream (Oksrukuyik Creek) where we observed Fe( ii ) and soluble Fe( iii ) in a highly reducing environment. The variable distribution of redox-active substances at all the sites yields insights into the nature and distribution of the important terminal electron acceptors in both lacustrine and tundra environments capable of exerting significant influences on the carbon cycle. 

Abstract The ocean–atmosphere exchange of CO 2 largely depends on the balance between marine microbial photosynthesis and respiration. Despite vast taxonomic and metabolic diversity among marine planktonic bacteria and archaea (prokaryoplankton) 1–3 , their respiration usually is measured in bulk and treated as a ‘black box’ in global biogeochemical models 4 ; this limits the mechanistic understanding of the global carbon cycle. Here, using a technology for integrated phenotype analyses and genomic sequencing of individual microbial cells, we show that cell-specific respiration rates differ by more than 1,000× among prokaryoplankton genera. The majority of respiration was found to be performed by minority members of prokaryoplankton (including the Roseobacter cluster), whereas cells of the most prevalent lineages (including Pelagibacter and SAR86) had extremely low respiration rates. The decoupling of respiration rates from abundance among lineages, elevated counts of proteorhodopsin transcripts in Pelagibacter and SAR86 cells and elevated respiration of SAR86 at night indicate that proteorhodopsin-based phototrophy 3,5–7 probably constitutes an important source of energy to prokaryoplankton and may increase growth efficiency. These findings suggest that the dependence of prokaryoplankton on respiration and remineralization of phytoplankton-derived organic carbon into CO 2 for its energy demands and growth may be lower than commonly assumed and variable among lineages. 

Twisted stalks are morphologically unique bacterial extracellular organo-metallic structures containing Fe(III) oxyhydroxides that are produced by microaerophilic Fe(II)-oxidizers belonging to the Betaproteobacteria and Zetaproteobacteria. Understanding the underlying genetic and physiological mechanisms of stalk formation is of great interest based on their potential as novel biogenic nanomaterials and their relevance as putative biomarkers for microbial Fe(II) oxidation on ancient Earth. Despite the recognition of these special biominerals for over 150 years, the genetic foundation for the stalk phenotype has remained unresolved. Here we present a candidate gene cluster for the biosynthesis and secretion of the stalk organic matrix that we identified with a trait-based analyses of a pan-genome comprising 16 Zetaproteobacteria isolate genomes. The “ s talk f ormation in Z etaproteobacteria” (sfz) cluster comprises six genes ( sfz1-sfz6 ), of which sfz1 and sfz2 were predicted with functions in exopolysaccharide synthesis, regulation, and export, sfz4 and sfz6 with functions in cell wall synthesis manipulation and carbohydrate hydrolysis, and sfz3 and sfz5 with unknown functions. The stalk-forming Betaproteobacteria Ferriphaselus R-1 and OYT-1, as well as dread-forming Zetaproteobacteria Mariprofundus aestuarium CP-5 and Mariprofundus ferrinatatus CP-8 contain distant sfz gene homologs, whereas stalk-less Zetaproteobacteria and Betaproteobacteria lack the entire gene cluster. Our pan-genome analysis further revealed a significant enrichment of clusters of orthologous groups (COGs) across all Zetaproteobacteria isolate genomes that are associated with the regulation of a switch between sessile and motile growth controlled by the intracellular signaling molecule c-di-GMP. Potential interactions between stalk-former unique transcription factor genes, sfz genes, and c-di-GMP point toward a c-di-GMP regulated surface attachment function of stalks during sessile growth.