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Human civilization relies on estuaries, and many estuarine ecosystem services are provided by microbial communities. These services include high rates of primary production that nourish harvests of commercially valuable species through fisheries and aquaculture, the transformation of terrestrial and anthropogenic materials to help ensure the water quality necessary to support recreation and tourism, and mutualisms that maintain blue carbon accumulation and storage. Research on the ecology that underlies microbial ecosystem services in estuaries has expanded greatly across a range of estuarine environments, including water, sediment, biofilms, biological reefs, and stands of seagrasses, marshes, and mangroves. Moreover, the application of new molecular tools has improved our understanding of the diversity and genomic functions of estuarine microbes. This review synthesizes recent research on microbial habitats in estuaries and the contributions of microbes to estuarine food webs, elemental cycling, and interactions with plants and animals, and highlights novel insights provided by recent advances in genomics. 

Salt marshes sit at the terrestrial–aquatic interface of oceans around the world. Unique features of salt marshes that differentiate them from their upland or offshore counterparts include high rates of primary production from vascular plants and saturated saline soils that lead to sharp redox gradients and a diversity of electron acceptors and donors. Moreover, the dynamic nature of root oxygen loss and tidal forcing leads to unique biogeochemical conditions that promote nitrogen cycling. Here, we highlight recent advances in our understanding of key nitrogen cycling processes in salt marshes and discuss areas where additional research is needed to better predict how salt marsh N cycling will respond to future environmental change. 

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 Excess reactive nitrogen (N) flows from agricultural, suburban, and urban systems to coasts, where it causes eutrophication. Coastal wetlands take up some of this N, thereby ameliorating the impacts on nearshore waters. Although the consequences of N on coastal wetlands have been extensively studied, the effect of the specific form of N is not often considered. Both oxidized N forms (nitrate, NO3−) and reduced forms (ammonium, NH4+) can relieve nutrient limitation and increase primary production. However, unlike NH4+, NO3− can also be used as an electron acceptor for microbial respiration. We present results demonstrating that, in salt marshes, microbes use NO3− to support organic matter decomposition and primary production is less stimulated than when enriched with reduced N. Understanding how different forms of N mediate the balance between primary production and decomposition is essential for managing coastal wetlands as N enrichment and sea level rise continue to assail our coasts. 

Abstract Nutrient enrichment impacts ecosystems globally. Population history, especially past resource environments, of numerically dominant plant species may affect their responses to subsequent changes in nutrient availability. Eutrophication can also alter plant–microbe interactions via direct effects on associated microbial communities or indirect effects on dominant species’ biomass production/allocation as a result of modified plant–soil interactions.We combined a greenhouse common garden and a field reciprocal transplant of a salt marsh foundation species (Spartina alterniflora) within a long‐term, whole‐ecosystem, nutrient‐enrichment study to determine whether enrichment affects plant production and microbial community structure differently depending on plant population history. For the greenhouse portion, we collected 20S. alternifloragenotypes—10 from an enriched creek that had received elevated nutrient inputs for 10 years and 10 from an unenriched reference creek—and reared them in a common garden for 1 year. For the field portion, we conducted a 2‐year, fully crossed reciprocal transplant experiment with two gardens each at the enriched and unenriched sites; we examined the effects of source site (i.e. population history), garden site and plant genotype.After 2 years, plants in enriched gardens had higher above‐ground biomass and altered below‐ground allocation compared to plants in unenriched gardens. However, performance also depended on plant population history: plants from the enriched site had decreased above‐ground and rhizome production compared to plants from the unenriched site, most notably in unenriched gardens. In addition, almost all above‐ and below‐ground traits varied depending on plant genotypic identity.Effects of nutrient enrichment on the associated microbial community were also pronounced. Following 1 year in common garden, microbial community structure varied by plant population history andS. alternifloragenotypic identity. However, at the end of the reciprocal transplant, microbial communities differed primarily between enriched and unenriched gardens.Synthesis. Nutrient enrichment can impact plant foundation species and associated soil microbes in the short term. Most importantly, nutrient enrichment can also have long‐lasting effects on plant populations and associated microbial communities that potentially compromise their ability to respond to changing resource conditions in the future. 

Metagenomes encode an enormous diversity of proteins, reflecting a multiplicity of functions and activities. Exploration of this vast sequence space has been limited to a comparative analysis against reference microbial genomes and protein families derived from those genomes. Here, to examine the scale of yet untapped functional diversity beyond what is currently possible through the lens of reference genomes, we develop a computational approach to generate reference-free protein families from the sequence space in metagenomes. We analyze 26,931 metagenomes and identify 1.17 billion protein sequences longer than 35 amino acids with no similarity to any sequences from 102,491 reference genomes or the Pfam database. Using massively parallel graph-based clustering, we group these proteins into 106,198 novel sequence clusters with more than 100 members, doubling the number of protein families obtained from the reference genomes clustered using the same approach. We annotate these families on the basis of their taxonomic, habitat, geographical, and gene neighborhood distributions and, where sufficient sequence diversity is available, predict protein three-dimensional models, revealing novel structures. Overall, our results uncover an enormously diverse functional space, highlighting the importance of further exploring the microbial functional dark matter.