Abstract Background Salt 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. Results A 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 . Conclusions The 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 detoxifies sulfide in the root zone while potentially transferring fixed C and N to the host plant.
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Microbial chemolithoautotrophs are abundant in salt marsh sediment following long-term experimental nitrate enrichment
Long-term anthropogenic nitrate (NO3−) enrichment is a serious threat to many coastal systems. Nitrate reduction coupled with the oxidation of reduced forms of sulfur is conducted by chemolithoautotrophic microbial populations in a process that decreases nitrogen (N) pollution. However, little is known about the diversity and distribution of microbes capable of carbon fixation within salt marsh sediment and how they respond to long-term NO3− loading. We used genome-resolved metagenomics to characterize the distribution, phylogenetic relationships, and adaptations important to microbial communities within NO3−-enriched sediment. We found NO3− reducing sulfur oxidizers became dominant members of the microbial community throughout the top 25 cm of the sediment following long-term NO3− enrichment. We also found that most of the chemolithoautotrophic genomes recovered contained striking metabolic versatility, including the potential for complete denitrification and evidence of mixotrophy. Phylogenetic reconstruction indicated that similar carbon fixation strategies and metabolic versatility can be found in several phylogenetic groups, but the genomes recovered here represent novel organisms. Our results suggest that the role of chemolithoautotrophy within NO3−-enriched salt marsh sediments may be quantitatively more important for retaining carbon and filtering NO3− than previously indicated and further inquiry is needed to explicitly measure their contribution to carbon turnover and removal of N pollution.
more » « less- NSF-PAR ID:
- 10446985
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- FEMS Microbiology Letters
- Volume:
- 370
- ISSN:
- 1574-6968
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Salt marshes sequester carbon at rates more than an order of magnitude greater than their terrestrial counterparts, helping to mitigate climate change. As nitrogen loading to coastal waters continues, primarily in the form of nitrate, it is unclear what effect it will have on carbon storage capacity of these highly productive systems. This uncertainty is largely driven by the dual role nitrate can play in biological processes, where it can serve as a nutrient‐stimulating primary production or a thermodynamically favorable electron acceptor fueling heterotrophic metabolism. Here, we used a controlled flow‐through reactor experiment to test the role of nitrate as an electron acceptor, and its effect on organic matter decomposition and the associated microbial community in salt marsh sediments. Organic matter decomposition significantly increased in response to nitrate, even at sediment depths typically considered resistant to decomposition. The use of isotope tracers suggests that this pattern was largely driven by stimulated denitrification. Nitrate addition also significantly altered the microbial community and decreased alpha diversity, selecting for taxa belonging to groups known to reduce nitrate and oxidize more complex forms of organic matter. Fourier Transform‐Infrared Spectroscopy further supported these results, suggesting that nitrate facilitated decomposition of complex organic matter compounds into more bioavailable forms. Taken together, these results suggest the existence of organic matter pools that only become accessible with nitrate and would otherwise remain stabilized in the sediment. The existence of such pools could have important implications for carbon storage, since greater decomposition rates as N loading increases may result in less overall burial of organic‐rich sediment. Given the extent of nitrogen loading along our coastlines, it is imperative that we better understand the resilience of salt marsh systems to nutrient enrichment, especially if we hope to rely on salt marshes, and other blue carbon systems, for long‐term carbon storage.
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Glass, Jennifer B. (Ed.)more » « less
ABSTRACT Sulfur-cycling microbial communities in salt marsh rhizosphere sediments mediate a recycling and detoxification system central to plant productivity. Despite the importance of sulfur-cycling microbes, their biogeographic, phylogenetic, and functional diversity remain poorly understood. Here, we use metagenomic data sets from Massachusetts (MA) and Alabama (AL) salt marshes to examine the distribution and genomic diversity of sulfur-cycling plant-associated microbes. Samples were collected from sediments under
Sporobolus alterniflorus andSporobolus pumilus in separate MA vegetation zones, and underS. alterniflorus andJuncus roemerianus co-occuring in AL. We grouped metagenomic data by plant species and site and identified 38 MAGs that included pathways for sulfate reduction or sulfur oxidation. Phylogenetic analyses indicated that 29 of the 38 were affiliated with uncultivated lineages. We showed differentiation in the distribution of MAGs between AL and MA, betweenS. alterniflorus andS. pumilus vegetation zones in MA, but no differentiation betweenS. alterniflorus andJ. roemerianus in AL. Pangenomic analyses of eight ubiquitous MAGs also detected site- and vegetation-specific genomic features, including varied sulfur-cycling operons, carbon fixation pathways, fixed single-nucleotide variants, and active diversity-generating retroelements. This genetic diversity, detected at multiple scales, suggests evolutionary relationships affected by distance and local environment, and demonstrates differential microbial capacities for sulfur and carbon cycling in salt marsh sediments.IMPORTANCE Salt marshes are known for their significant carbon storage capacity, and sulfur cycling is closely linked with the ecosystem-scale carbon cycling in these ecosystems. Sulfate reducers are key for the decomposition of organic matter, and sulfur oxidizers remove toxic sulfide, supporting the productivity of marsh plants. To date, the complexity of coastal environments, heterogeneity of the rhizosphere, high microbial diversity, and uncultured majority hindered our understanding of the genomic diversity of sulfur-cycling microbes in salt marshes. Here, we use comparative genomics to overcome these challenges and provide an in-depth characterization of sulfur-cycling microbial diversity in salt marshes. We characterize communities across distinct sites and plant species and uncover extensive genomic diversity at the taxon level and specific genomic features present in MAGs affiliated with uncultivated sulfur-cycling lineages. Our work provides insights into the partnerships in salt marshes and a roadmap for multiscale analyses of diversity in complex biological systems.
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null (Ed.)Deep subsurface environments are decoupled from Earth’s surface processes yet diverse, active, and abundant microbial communities thrive in these isolated environments. Microbes inhabiting the deep biosphere face unique challenges such as electron donor/acceptor limitations, pore space/fracture network limitations, and isolation from other microbes within the formation. Of the few systems that have been characterized, it is apparent that nutrient limitations likely facilitate diverse microbe-microbe interactions (i.e., syntrophic, symbiotic, or parasitic) and that these interactions drive biogeochemical cycling of major elements. Here we describe microbial communities living in low temperature, chemically reduced brines at the Soudan Underground Mine State Park, United States. The Soudan Iron mine intersects a massive hematite formation at the southern extent of the Canadian Shield. Fractured rock aquifer brines continuously flow from exploratory boreholes drilled circa 1960 and are enriched in deuterium compared to the global meteoric values, indicating brines have had little contact with surface derived waters, and continually degas low molecular weight hydrocarbons C 1 -C 4 . Microbial enrichments suggest that once brines exit the boreholes, oxidation of the hydrocarbons occur. Amplicon sequencing show these borehole communities are low in diversity and dominated by Firmicute and Proteobacteria phyla. From the metagenome assemblies, we recovered approximately thirty genomes with estimated completion over 50%. Analysis of genome taxonomy generally followed the amplicon data, and highlights that several of the genomes represent novel families and genera. Metabolic reconstruction shows two carbon-fixation pathways were dominant, the Wood-Ljungdahl (acetogenesis) and Calvin-Benson-Bassham (via RuBisCo), indicating that inorganic carbon likely enters into the microbial foodweb with differing carbon fractionation potentials. Interestingly, methanogenesis is likely driven by Methanolobus and suggests cycling of methylated compounds and not H 2 /CO 2 or acetate. Furthermore, the abundance of sulfate in brines suggests cryptic sulfur cycling may occur, as we detect possible sulfate reducing and thiosulfate oxidizing microorganisms. Finally, a majority of the microorganisms identified contain genes that would allow them to participate in several element cycles, highlighting that in these deep isolated systems metabolic flexibility may be an important life history trait.more » « less
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Abstract High‐throughput sequencing has enabled robust shotgun metagenomic sequencing that informs our understanding of the genetic basis of important biogeochemical processes. Slower to develop, however, are the application of these tools in a controlled experimental framework that pushes the field beyond exploratory analysis toward hypothesis‐driven research. We performed flow‐through reactor experiments to examine how salt marsh sediments from varying depths respond to nitrate addition and linked biogeochemical processes to this underlying genetic foundation. Understanding the mechanistic basis of carbon and nitrogen cycling in salt marsh sediments is critical for predicting how important ecosystem services provided by marshes, including carbon storage and nutrient removal, will respond to global change. Prior to the addition of nitrate, we used metagenomics to examine the functional potential of the sediment microbial community that occurred along a depth gradient, where organic matter reactivity changes due to decomposition. Metagenomic data indicated that genes encoding enzymes involved in respiration, including denitrification, were higher in shallow sediments, and genes indicative of resource limitation were greatest at depth. After 92 d of nitrate enrichment, we measured cumulative increases in dissolved inorganic carbon production, denitrification, and dissimilatory nitrate reduction to ammonium; these rates correlated strongly with genes that encode essential enzymes in these important pathways. Our results highlight the importance of controlled experiments in linking biogeochemical rates to underlying genetic pathways. Furthermore, they indicate the importance of nitrate as an electron acceptor in fueling microbial respiration, which has consequences for carbon and nitrogen cycling and fate in coastal marine systems.
