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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 underSporobolus alterniflorusandSporobolus pumilusin separate MA vegetation zones, and underS. alterniflorusandJuncus roemerianusco-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. alterniflorusandS. pumilusvegetation zones in MA, but no differentiation betweenS. alterniflorusandJ. roemerianusin 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. IMPORTANCESalt 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. 

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.