Heterotrophic activity, primarily driven by sulfate-reducing prokaryotes, has traditionally been linked to nitrogen fixation in the root zone of coastal marine plants, leaving the role of chemolithoautotrophy in this process unexplored. Here, we show that sulfur oxidation coupled to nitrogen fixation is a previously overlooked process providing nitrogen to coastal marine macrophytes. In this study, we recovered 239 metagenome-assembled genomes from a salt marsh dominated by the foundation plant
- PAR ID:
- 10355721
- Date Published:
- Journal Name:
- Microbiome
- Volume:
- 10
- Issue:
- 1
- ISSN:
- 2049-2618
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Spartina alterniflora , including diazotrophic sulfate-reducing and sulfur-oxidizing bacteria. Abundant sulfur-oxidizing bacteria encode and highly express genes for carbon fixation (RuBisCO ), nitrogen fixation (nifHDK ) and sulfur oxidation (oxidative-dsrAB ), especially in roots stressed by sulfidic and reduced sediment conditions. Stressed roots exhibited the highest rates of nitrogen fixation and expression level of sulfur oxidation and sulfate reduction genes. Close relatives of marine symbionts from theCandidatus Thiodiazotropha genus contributed ~30% and ~20% of all sulfur-oxidizingdsrA and nitrogen-fixingnifK transcripts in stressed roots, respectively. Based on these findings, we propose that the symbiosis betweenS. alterniflora and sulfur-oxidizing bacteria is key to ecosystem functioning of coastal salt marshes. -
Shade, Ashley (Ed.)ABSTRACT We develop a method to artificially select for rhizosphere microbiomes that confer salt tolerance to the model grass Brachypodium distachyon grown under sodium salt stress or aluminum salt stress. In a controlled greenhouse environment, we differentially propagated rhizosphere microbiomes between plants of a nonevolving, highly inbred plant population; therefore, only microbiomes evolved in our experiment, but the plants did not evolve in parallel. To maximize microbiome perpetuation when transplanting microbiomes between plants and, thus, maximize response to microbiome selection, we improved earlier methods by (i) controlling microbiome assembly when inoculating seeds at the beginning of each selection cycle; (ii) fractionating microbiomes before transfer between plants to harvest, perpetuate, and select on only bacterial and viral microbiome components; (iii) ramping of salt stress gradually from minor to extreme salt stress with each selection cycle to minimize the chance of overstressing plants; (iv) using two nonselection control treatments (e.g., nonselection microbial enrichment and null inoculation) that permit comparison to the improving fitness benefits that selected microbiomes impart on plants. Unlike previous methods, our selection protocol generated microbiomes that enhance plant fitness after only 1 to 3 rounds of microbiome selection. After nine rounds of microbiome selection, the effect of microbiomes selected to confer tolerance to aluminum salt stress was nonspecific (these artificially selected microbiomes equally ameliorate sodium and aluminum salt stresses), but the effect of microbiomes selected to confer tolerance to sodium salt stress was specific (these artificially selected microbiomes do not confer tolerance to aluminum salt stress). Plants with artificially selected microbiomes had 55 to 205% greater seed production than plants with unselected control microbiomes. IMPORTANCE We developed an experimental protocol that improves earlier methods of artificial selection on microbiomes and then tested the efficacy of our protocol to breed root-associated bacterial microbiomes that confer salt tolerance to a plant. Salt stress limits growth and seed production of crop plants, and artificially selected microbiomes conferring salt tolerance may ultimately help improve agricultural productivity. Unlike previous experiments of microbiome selection, our selection protocol generated microbiomes that enhance plant productivity after only 1 to 3 rounds of artificial selection on root-associated microbiomes, increasing seed production under extreme salt stress by 55 to 205% after nine rounds of microbiome selection. Although we artificially selected microbiomes under controlled greenhouse conditions that differ from outdoor conditions, increasing seed production by 55 to 205% under extreme salt stress is a remarkable enhancement of plant productivity compared to traditional plant breeding. We describe a series of additional experimental protocols that will advance insights into key parameters that determine efficacy and response to microbiome selection.more » « less
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Abstract Plant identity and cover in coastal wetlands is changing in worldwide, and many subtropical salt marshes dominated by low‐stature herbaceous species are becoming woody mangroves. Yet, how changes affect coastal soil biogeochemical processes and belowground biomass before and after storms is uncertain. We experimentally manipulated the percent mangrove cover (
Avicennia germinans ) in 3 × 3 m cells embedded in 10 plots (24 × 42 m) comprising a gradient of marsh (e.g.,Spartina alterniflora ,Batis maritima ) and mangrove cover in Texas, USA. Hurricane Harvey made direct landfall over our site on 25 August 2017, providing a unique opportunity to test how plant composition mitigates hurricane effects on surface sediment accretion, soil chemistry (carbon, C; nitrogen, N; phosphorus, P; and sulfur, S), and root biomass. Data were collected before (2013 and 2016), one‐month after (2017), and one‐year after (2018) Hurricane Harvey crossed the area, allowing us to measure stocks before and after the hurricane. The accretion depth was higher in fringe compared with interior cells of plots, more variable in cells dominated by marsh than mangrove, and declined with increasing plot‐scale mangrove cover. The concentrations of P and δ34S in storm‐driven accreted surface sediments, and the concentrations of N, P, S, and δ34S in underlying soils (0–30 cm), decreased post‐hurricane, whereas the C concentrations in both compartments were unchanged. Root biomass in both marsh and mangrove cells was reduced by 80% in 2017 compared with previous dates and remained reduced in 2018. Post‐hurricane loss of root biomass in plots correlated with enhanced nutrient limitation. Total sulfide accumulation as indicated by δ34S, increased nutrient limitation, and decreased root biomass of both marshes and mangroves after hurricanes may affect ecosystem function and increase vulnerability in coastal wetlands to subsequent disturbances. Understanding how changes in plant composition in coastal ecosystems affects responses to hurricane disturbances is needed to assess coastal vulnerability. -
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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 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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Marsh elevation was measured with a Surface Elevation Table (SET) as a component of a long-term project seeking to understand how salt marsh primary production and sediment chemistry respond to anthropogenic (e.g. eutrophication) and natural (e.g. sea-level rise) environmental change. Feedbacks between plants, sediments, nutrients and flooding were investigated with particular attention to mechanisms that keep marshes in equilibrium with sea level. Other data collected as part of the project include aboveground annual primary productivity, plant biomass, plant density and porewater nutrient concentrations. These data have been used to develop the Marsh Equilibrium Model, an important tool for coastal resource managers. Sampling occurred at 7 Spartina alterniflora-dominated salt marsh sites in North Inlet, a relatively pristine estuary near Georgetown, SC on the SE coast of the United States. North Inlet is a tidally-dominated, bar-built estuary, with a semi-diurnal mixed tide and a tidal range of 1.4m. The 25-km2 estuary is comprised of about 20.5 km2 of intertidal salt marsh and mudflats, and 4.5 km2 of open water. Marsh elevation sampling began in 1990, 1991, 1996 or 2000, depending on the site. Sampling occurred approximately monthly or approximately annually through 2022. The study is on-going. Additionally, some plots were fertilized with nitrogen and phosphorus.more » « less
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1186/s40168-021-01187-7
