skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.

Explore Research Products in the PAR
It may take a few hours for recently added research products to appear in PAR search results.


Title: Diversity at single nucleotide to pangenome scales among sulfur cycling bacteria in salt marshes
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.  more » « less
Award ID(s):
2224608
PAR ID:
10502243
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ;
Editor(s):
Glass, Jennifer B.
Publisher / Repository:
AEM
Date Published:
Journal Name:
Applied and Environmental Microbiology
Volume:
89
Issue:
11
ISSN:
0099-2240
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; ; ; (, mSystems)
    Wilkins, Laetitia_G E (Ed.)
    ABSTRACT Anaerolineae, particularly uncultured representatives, are one of the most abundant microbial groups in coastal salt marshes, dominating the belowground rhizosphere, where over half of plant biomass production occurs. However, this class generally remains poorly understood, particularly in a salt marsh context. Here, novelAnaerolineaemetagenome-assembled genomes (MAGs) were generated from the salt marsh rhizosphere representingAnaerolineales,Promineifilales, JAAYZQ01, B4-G1, JAFGEY01, UCB3, andCaldilinealesorders. Metagenome and metatranscriptome reads were mapped to annotated MAGs, revealing nearly allAnaerolineaeencoded and transcribed genes required for oxidation of carbon compounds ranging from simple sugars to complex polysaccharides, fermentation, and carbon fixation. Furthermore, the majority ofAnaerolineaeexpressed genes involved in anaerobic and aerobic respiration and secondary metabolite production. The data revealed that the belowground salt marshAnaerolineaein the rhizosphere are important players in carbon cycling, including degradation of simple carbon compounds and more recalcitrant plant material, such as cellulose, using a diversity of electron acceptors and represent an unexplored reservoir of novel secondary metabolites.IMPORTANCEGiven that coastal salt marshes are recognized as biogeochemical hotspots, it is fundamentally important to understand the functional role of the microbiome in this ecosystem. In particular,Anaerolineaeare abundant members of the salt marsh rhizosphere and have been identified as core microbes, suggesting they play an important functional role. Yet, little is known about the metabolic pathways encoded and expressed in this abundant salt marsh clade. Using an ‘omics-based approach, we determined thatAnaerolineaeare capable of oxidizing a range of carbon compounds, including simple sugars to complex carbon compounds, while also encoding fermentation and carbon fixation. Surprisingly,Anaerolineaeencoded and transcribed genes involved in aerobic respiration, which was unexpected given the reduced nature of the salt marsh rhizosphere. Finally, the majority ofAnaerolineaeappear to be involved in secondary metabolite production, suggesting that this group represents an unexplored reservoir of novel and important secondary metabolites. 
    more » « less
  2. ; ; ; ; ; ; ; ; (, Biogeochemistry)
    Abstract Salt marshes can attenuate nutrient pollution and store large amounts of ‘blue carbon’ in their soils, however, the value of sequestered carbon may be partially offset by nitrous oxide (N2O) emissions. Global climate and land use changes result in higher temperatures and inputs of reactive nitrogen (Nr) into coastal zones. Here, we investigated the combined effects of elevated temperature (ambient + 5℃) and Nr (double ambient concentrations) on nitrogen processing in marsh soils from two climatic regions (Quebec, Canada and Louisiana, U.S.) with two vegetation types,Sporobolus alterniflorus(= Spartina alterniflora) andSporobolus pumilus(= Spartina patens), using 24-h laboratory incubation experiments. Potential N2O fluxes increased from minor sinks to major sources following elevated treatments across all four marsh sites. One day of potential N2O emissions under elevated treatments (representing either long-term sea surface warming or short-term ocean heatwaves effects on coastal marsh soil temperatures alongside pulses of N loading) offset 15–60% of the potential annual ambient N2O sink, depending on marsh site and vegetation type. Rates of potential denitrification were generally higher in high latitude than in low latitude marsh soils under ambient treatments, with low ratios of N2O:N2indicating complete denitrification in high latitude marsh soils. Under elevated temperature and Nr treatments, potential denitrification was lower in high latitude soil but higher in low latitude soil as compared to ambient conditions, with incomplete denitrification observed except in LouisianaS. pumilus. Overall, our findings suggest that a combined increase in temperature and Nr has the potential to reduce salt marsh greenhouse gas (GHG) sinks under future global change scenarios. 
    more » « less
  3. ; ; ; ; ; (, Restoration Ecology)
    Thin layer sediment placement (TLP) is used to build elevation in marshes, counteracting effects of subsidence and sea level rise. However, TLP success may vary due to plant stress associated with reductions in nutrient availability and hydrologic flushing or through the creation of acid sulfate soils. This study examined the influence of sediment grain size and soil amendments on plant growth, soil and porewater characteristics, and greenhouse gas exchange for three key U.S. salt marsh plants:Spartina alterniflora(synonymSporobolus alterniflorus),Spartina patens(synonymSporobolus pumilus), andSalicornia pacifica.We found that bioavailable nitrogen concentrations (measured as extractable NH4+‐N) and porewater pH and salinity were inversely related to grain size, while soil redox was more reducing in finer sediments. This suggests that utilizing finer sediments in TLP projects will result in a more reduced environment with higher nutrient availability, while larger grain sized sediments will be better flushed and oxygenated. We further found that grain size had a significant effect on vegetation biomass allocation and rates of gas exchange, although these effects were species‐specific. We found that soil amendments (biochar and compost) did not subsidize plant growth but were associated with increases in soil respiration and methane emissions. Biochar amendments were additionally ineffective in ameliorating acid sulfate conditions. This study uncovers complex interactions between sediment type and vegetation, emphasizing the limitations of soil amendments. The findings aid restoration project managers in making informed decisions regarding sediment type, target vegetation, and soil amendments for successful TLP projects. 
    more » « less
  4. ; ; ; (, ISME communications)
    Studies on microbial sulfur cycling in marine sediment have primarily centered on the cycling of inorganic sulfur. The microbial diversity underlying the cycling of organosulfur compounds is largely unexplored. In this study, we present the first quantification of dissolved organic sulfur (DOS) microbial assimilation in marine surface sediments using 13C-DOS quantitative DNA stable isotope probing (qSIP). We sampled marine sediment from 493 m water depth on the Puerto Rico continental slope, measured 13C-assimilation from two DOS substrates (13C-taurine and 13C-methionine), and compared the 13C-DOS assimilation to 13C-glucose uptake. Taurine utilization was confined to bacteria, whereas methionine was degraded by bacteria and archaea, including methanogenic Methanococcoides. Globally widespread uncultivated clades of Gammaproteobacteria and Deltaproteobacteria were the main drivers of DOS cycling and exhibited increased assimilation of carbon from taurine and methionine, compared to glucose. Only one operational taxonomic unit (OTU) affiliated with Neptuniibacter was found to assimilate taurine and methionine, but not glucose, implying that microbes exclusively utilizing both DOS substrates as a carbon source in marine sediments are rare. Still, a substantial number of bacterial taxa exhibited a higher assimilation of 13C from taurine or methionine, compared to glucose, indicating their preference for both DOS substrates over glucose as a carbon source in the sediment. These results represent the first quantitative assessment of organosulfur cycling from taurine and methionine by uncultivated microbes in a marine benthic environment. 
    more » « less
  5. ; ; ; ; (, Frontiers in Microbiology)
    Hydrothermal sediments host phylogenetically diverse and physiologically complex microbial communities. Previous studies of microbial community structure in hydrothermal sediments have typically used short-read sequencing approaches. To improve on these approaches, we use LoopSeq, a high-throughput synthetic long-read sequencing method that has yielded promising results in analyses of microbial ecosystems, such as the human gut microbiome. In this study, LoopSeq is used to obtain near-full length (approximately 1,400–1,500 nucleotides) bacterial 16S rRNA gene sequences from hydrothermal sediments in Guaymas Basin. Based on these sequences, high-quality alignments and phylogenetic analyses provided new insights into previously unrecognized taxonomic diversity of sulfur-cycling microorganisms and their distribution along a lateral hydrothermal gradient. Detailed phylogenies for free-living and syntrophic sulfur-cycling bacterial lineages identified well-supported monophyletic clusters that have implications for the taxonomic classification of these groups. Particularly, we identify clusters withinCandidatusDesulfofervidus that represent unexplored physiological and genomic diversity. In general, LoopSeq-derived 16S rRNA gene sequences aligned consistently with reference sequences in GenBank; however, chimeras were prevalent in sequences as affiliated with the thermophilicCandidatusDesulfofervidus andThermodesulfobacterium, and in smaller numbers within the sulfur-oxidizing familyBeggiatoaceae. Our analysis of sediments along a well-documented thermal and geochemical gradient show how lineages affiliated with different sulfur-cycling taxonomic groups persist throughout surficial hydrothermal sediments in the Guaymas Basin. 
    more » « less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email