skip to main content

This content will become publicly available on December 1, 2023

Title: The core root microbiome of Spartina alterniflora is predominated by sulfur-oxidizing and sulfate-reducing bacteria in Georgia salt marshes, USA
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 more » 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. « less
; ; ;
Award ID(s):
Publication Date:
Journal Name:
Sponsoring Org:
National Science Foundation
More Like this
  1. Martiny, Jennifer B. (Ed.)
    ABSTRACT Peat mosses of the genus Sphagnum are ecosystem engineers that frequently predominate over photosynthetic production in boreal peatlands. Sphagnum spp. host diverse microbial communities capable of nitrogen fixation (diazotrophy) and methane oxidation (methanotrophy), thereby potentially supporting plant growth under severely nutrient-limited conditions. Moreover, diazotrophic methanotrophs represent a possible “missing link” between the carbon and nitrogen cycles, but the functional contributions of the Sphagnum -associated microbiome remain in question. A combination of metagenomics, metatranscriptomics, and dual-isotope incorporation assays was applied to investigate Sphagnum microbiome community composition across the North American continent and provide empirical evidence for diazotrophic methanotrophy in Sphagnum -dominated ecosystems. Remarkably consistent prokaryotic communities were detected in over 250 Sphagnum SSU rRNA libraries from peatlands across the United States (5 states, 17 bog/fen sites, 18 Sphagnum species), with 12 genera of the core microbiome comprising 60% of the relative microbial abundance. Additionally, nitrogenase ( nifH ) and SSU rRNA gene amplicon analysis revealed that nitrogen-fixing populations made up nearly 15% of the prokaryotic communities, predominated by Nostocales cyanobacteria and Rhizobiales methanotrophs. While cyanobacteria comprised the vast majority (>95%) of diazotrophs detected in amplicon and metagenome analyses, obligate methanotrophs of the genus Methyloferula (order Rhizobiales ) accounted for one-quartermore »of transcribed nifH genes. Furthermore, in dual-isotope tracer experiments, members of the Rhizobiales showed substantial incorporation of 13 CH 4 and 15 N 2 isotopes into their rRNA. Our study characterizes the core Sphagnum microbiome across large spatial scales and indicates that diazotrophic methanotrophs, here defined as obligate methanotrophs of the rare biosphere ( Methyloferula spp. of the Rhizobiales ) that also carry out diazotrophy, play a keystone role in coupling of the carbon and nitrogen cycles in nutrient-poor peatlands. IMPORTANCE Nitrogen availability frequently limits photosynthetic production in Sphagnum moss-dominated high-latitude peatlands, which are crucial carbon-sequestering ecosystems at risk to climate change effects. It has been previously suggested that microbial methane-fueled fixation of atmospheric nitrogen (N 2 ) may occur in these ecosystems, but this process and the organisms involved are largely uncharacterized. A combination of omics (DNA and RNA characterization) and dual-isotope incorporation approaches illuminated the functional diversity of Sphagnum -associated microbiomes and defined 12 bacterial genera in its core microbiome at the continental scale. Moreover, obligate diazotrophic methanotrophs showed high nitrogen fixation gene expression levels and incorporated a substantial amount of atmospheric nitrogen and methane-driven carbon into their biomass. Thus, these results point to a central role for members of the rare biosphere in Sphagnum microbiomes as keystone species that couple nitrogen fixation to methane oxidation in nutrient-poor peatlands.« less
  2. 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 selectedmore »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.« less
  3. Campbell, Barbara J. (Ed.)
    ABSTRACT In nutrient-limited conditions, plants rely on rhizosphere microbial members to facilitate nutrient acquisition, and in return, plants provide carbon resources to these root-associated microorganisms. However, atmospheric nutrient deposition can affect plant-microbe relationships by changing soil bacterial composition and by reducing cooperation between microbial taxa and plants. To examine how long-term nutrient addition shapes rhizosphere community composition, we compared traits associated with bacterial (fast-growing copiotrophs, slow-growing oligotrophs) and plant (C 3 forb, C 4 grass) communities residing in a nutrient-poor wetland ecosystem. Results revealed that oligotrophic taxa dominated soil bacterial communities and that fertilization increased the presence of oligotrophs in bulk and rhizosphere communities. Additionally, bacterial species diversity was greatest in fertilized soils, particularly in bulk soils. Nutrient enrichment (fertilized versus unfertilized) and plant association (bulk versus rhizosphere) determined bacterial community composition; bacterial community structure associated with plant functional group (grass versus forb) was similar within treatments but differed between fertilization treatments. The core forb microbiome consisted of 602 unique taxa, and the core grass microbiome consisted of 372 unique taxa. Forb rhizospheres were enriched in potentially disease-suppressive bacterial taxa, and grass rhizospheres were enriched in bacterial taxa associated with complex carbon decomposition. Results from this study demonstrate that fertilizationmore »serves as a strong environmental filter on the soil microbiome, which leads to distinct rhizosphere communities and can shift plant effects on the rhizosphere microbiome. These taxonomic shifts within plant rhizospheres could have implications for plant health and ecosystem functions associated with carbon and nitrogen cycling. IMPORTANCE Over the last century, humans have substantially altered nitrogen and phosphorus cycling. Use of synthetic fertilizer and burning of fossil fuels and biomass have increased nitrogen and phosphorus deposition, which results in unintended fertilization of historically low-nutrient ecosystems. With increased nutrient availability, plant biodiversity is expected to decline, and the abundance of copiotrophic taxa is anticipated to increase in bacterial communities. Here, we address how bacterial communities associated with different plant functional types (forb, grass) shift due to long-term nutrient enrichment. Unlike other studies, results revealed an increase in bacterial diversity, particularly of oligotrophic bacteria in fertilized plots. We observed that nutrient addition strongly determines forb and grass rhizosphere composition, which could indicate different metabolic preferences in the bacterial communities. This study highlights how long-term fertilization of oligotroph-dominated wetlands could alter diversity and metabolism of rhizosphere bacterial communities in unexpected ways.« less
  4. Stams, Alfons J. (Ed.)
    ABSTRACT Hydrologic shifts due to climate change will affect the cycling of carbon (C) stored in boreal peatlands. Carbon cycling in these systems is carried out by microorganisms and plants in close association. This study investigated the effects of experimentally manipulated water tables (lowered and raised) and plant functional groups on the peat and root microbiomes in a boreal rich fen. All samples were sequenced and processed for bacterial, archaeal (16S DNA genes; V4), and fungal (internal transcribed spacer 2 [ITS2]) DNA. Depth had a strong effect on microbial and fungal communities across all water table treatments. Bacterial and archaeal communities were most sensitive to the water table treatments, particularly at the 10- to 20-cm depth; this area coincides with the rhizosphere or rooting zone. Iron cyclers, particularly members of the family Geobacteraceae , were enriched around the roots of sedges, horsetails, and grasses. The fungal community was affected largely by plant functional group, especially cinquefoils. Fungal endophytes (particularly Acephala spp.) were enriched in sedge and grass roots, which may have underappreciated implications for organic matter breakdown and cycling. Fungal lignocellulose degraders were enriched in the lowered water table treatment. Our results were indicative of two main methanogen communities, amore »rooting zone community dominated by the archaeal family Methanobacteriaceae and a deep peat community dominated by the family Methanomicrobiaceae . IMPORTANCE This study demonstrated that roots and the rooting zone in boreal fens support organisms likely capable of methanogenesis, iron cycling, and fungal endophytic association and are directly or indirectly affecting carbon cycling in these ecosystems. These taxa, which react to changes in the water table and associate with roots and, particularly, graminoids, may gain greater biogeochemical influence, as projected higher precipitation rates could lead to an increased abundance of sedges and grasses in boreal fens.« less
  5. International Ocean Discovery Program (IODP) Expedition 357 successfully cored an east–west transect across the southern wall of Atlantis Massif on the western flank of the Mid-Atlantic Ridge to study the links between serpentinization processes and microbial activity in the shallow subsurface of highly altered ultramafic and mafic sequences that have been uplifted to the seafloor along a major detachment fault zone. The primary goals of this expedition were to (1) examine the role of serpentinization in driving hydrothermal systems, sustaining microbial communities, and sequestering carbon; (2) characterize the tectonomagmatic processes that lead to lithospheric heterogeneities and detachment faulting; and (3) assess how abiotic and biotic processes change with variations in rock type and progressive exposure on the seafloor. To accomplish these objectives, we developed a coring and sampling strategy based around the use of seabed rock drills—the first time that such systems have been used in the scientific ocean drilling programs. This technology was chosen in hopes of achieving high recovery of the carbonate cap sequences and intact contact and deformation relationships. The expedition plans also included several engineering developments to assess geochemical parameters during drilling; sample bottom water before and after drilling; supply synthetic tracers during drilling for contaminationmore »assessment; gather downhole electrical resistivity and magnetic susceptibility logs for assessing fractures, fluid flow, and extent of serpentinization; and seal boreholes to provide opportunities for future experiments. Seventeen holes were drilled at nine sites across Atlantis Massif, with two sites on the eastern end of the southern wall (Sites M0068 and M0075), three sites in the central section of the southern wall north of the Lost City hydrothermal field (Sites M0069, M0072, and M0076), two sites on the western end (Sites M0071 and M0073), and two sites north of the southern wall in the direction of the central dome of the massif and Integrated Ocean Drilling Program Site U1309 (Sites M0070 and M0074). Use of seabed rock drills enabled collection of more than 57 m of core, with borehole penetration ranging from 1.3 to 16.44 meters below seafloor and core recoveries as high as 75% of total penetration. This high level of recovery of shallow mantle sequences is unprecedented in the history of ocean drilling. The cores recovered along the southern wall of Atlantis Massif have highly heterogeneous lithologies, types of alteration, and degrees of deformation. The ultramafic rocks are dominated by harzburgites with intervals of dunite and minor pyroxenite veins, as well as gabbroic rocks occurring as melt impregnations and veins, all of which provide information about early magmatic processes and the magmatic evolution in the southernmost portion of Atlantis Massif. Dolerite dikes and basaltic rocks represent the latest stage of magmatic activity. Overall, the ultramafic rocks recovered during Expedition 357 revealed a high degree of serpentinization, as well as metasomatic talc-amphibole-chlorite overprinting and local rodingitization. Metasomatism postdates an early phase of serpentinization but predates late-stage intrusion and alteration of dolerite dikes and the extrusion of basalt. The intensity of alteration is generally lower in the gabbroic and doleritic rocks. Chilled margins in dolerite intruded into talc-amphibole-chlorite schists are observed at the most eastern Site M0075. Deformation in Expedition 357 cores is variable and dominated by brecciation and formation of localized shear zones; the degree of carbonate veining was lower than anticipated. All types of variably altered and deformed ultramafic and mafic rocks occur as components in sedimentary breccias and as fault scarp rubble. The sedimentary cap rocks include basaltic breccias with a carbonate sand matrix and/or fossiliferous carbonate. Fresh glass on basaltic components was observed in some of the breccias. The expedition also successfully applied new technologies, namely (1) extensively using an in situ sensor package and water sampling system on the seabed drills for evaluating real-time dissolved oxygen and methane, pH, oxidation-reduction potential, temperature, and conductivity during drilling; (2) deploying a borehole plug system for sealing seabed drill boreholes at four sites to allow access for future sampling; and (3) proving that tracers can be delivered into drilling fluids when using seabed drills. The rock drill sensor packages and water sampling enabled detection of elevated dissolved methane and hydrogen concentrations during and/or after drilling, with “hot spots” of hydrogen observed over Sites M0068–M0072 and methane over Sites M0070–M0072. Shipboard determination of contamination tracer delivery confirmed appropriate sample handling procedures for microbiological and geochemical analyses, which will aid all subsequent microbiological investigations that are part of the science party sampling plans, as well as verify this new tracer delivery technology for seabed drill rigs. Shipboard investigation of biomass density in select samples revealed relatively low and variable cell densities, and enrichment experiments set up shipboard reveal growth. Thus, we anticipate achieving many of the deep biosphere–related objectives of the expedition through continued scientific investigation in the coming years. Finally, although not an objective of the expedition, we were serendipitously able to generate a high-resolution (20 m per pixel) multibeam bathymetry map across the entire Atlantis Massif and the nearby fracture zone, Mid-Atlantic Ridge, and eastern conjugate, taking advantage of weather and operational downtime. This will assist science party members in evaluating and interpreting tectonic and mass-wasting processes at Atlantis Massif.« less