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1. The core root microbiome of Spartina alterniflora is predominated by sulfur-oxidizing and sulfate-reducing bacteria in Georgia salt marshes, USA

   https://doi.org/10.1186/s40168-021-01187-7  

   Rolando, Jose L.; Kolton, Max; Song, Tianze; Kostka, Joel E. (December 2022, Microbiome)

   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 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. 

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2. Gallionellaceae in rice root plaque: metabolic roles in iron oxidation, nutrient cycling, and plant interactions

   https://doi.org/10.1128/aem.00570-23  

   Chan, Clara S.; Dykes, Gretchen E.; Hoover, Rene L.; Limmer, Matt A.; Seyfferth, Angelia L. (December 2023, Applied and Environmental Microbiology)

   Glass, Jennifer B. (Ed.)

   ABSTRACT On the roots of wetland plants such as rice, Fe(II) oxidation forms Fe(III) oxyhydroxide-rich plaques that modulate plant nutrient and metal uptake. The microbial roles in catalyzing this oxidation have been debated and it is unclear if these iron-oxidizers mediate other important biogeochemical and plant interactions. To investigate this, we studied the microbial communities, metagenomes, and geochemistry of iron plaque on field-grown rice, plus the surrounding rhizosphere and bulk soil. Plaque iron content (per mass root) increased over the growing season, showing continuous deposition. Analysis of 16S rRNA genes showed abundant Fe(II)-oxidizing and Fe(III)-reducing bacteria (FeOB and FeRB) in plaque, rhizosphere, and bulk soil. FeOB were enriched in relative abundance in plaque, suggesting FeOB affinity for the root surface. Gallionellaceae FeOBSideroxydanswere enriched during vegetative and early reproductive rice growth stages, while aGallionellawas enriched during reproduction through grain maturity, suggesting distinct FeOB niches over the rice life cycle. FeRBAnaeromyxobacterandGeobacterincreased in plaque later, during reproduction and grain ripening, corresponding to increased plaque iron. Metagenome-assembled genomes revealed that Gallionellaceae may grow mixotrophically using both Fe(II) and organics. TheSideroxydansare facultative, able to use non-Fe substrates, which may allow colonization of rice roots early in the season. FeOB genomes suggest adaptations for interacting with plants, including colonization, plant immunity defense, utilization of plant organics, and nitrogen fixation. Taken together, our results strongly suggest that rhizoplane and rhizosphere FeOB can specifically associate with rice roots, catalyzing iron plaque formation, with the potential to contribute to plant growth. IMPORTANCEIn waterlogged soils, iron plaque forms a reactive barrier between the root and soil, collecting phosphate and metals such as arsenic and cadmium. It is well established that iron-reducing bacteria solubilize iron, releasing these associated elements. In contrast, microbial roles in plaque formation have not been clear. Here, we show that there is a substantial population of iron oxidizers in plaque, and furthermore, that these organisms (SideroxydansandGallionella) are distinguished by genes for plant colonization and nutrient fixation. Our results suggest that iron-oxidizing and iron-reducing bacteria form and remodel iron plaque, making it a dynamic system that represents both a temporary sink for elements (P, As, Cd, C, etc.) as well as a source. In contrast to abiotic iron oxidation, microbial iron oxidation results in coupled Fe-C-N cycling, as well as microbe-microbe and microbe-plant ecological interactions that need to be considered in soil biogeochemistry, ecosystem dynamics, and crop management. 

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3. Diversity at single nucleotide to pangenome scales among sulfur cycling bacteria in salt marshes

   https://doi.org/10.1128/aem.00988-23  

   Pérez Castro, Sherlynette; Peredo, Elena L.; Mason, Olivia U.; Vineis, Joseph; Bowen, Jennifer L.; Mortazavi, Behzad; Ganesh, Anakha; Ruff, S. Emil; Paul, Blair G.; Giblin, Anne E.; et al (November 2023, Applied and Environmental Microbiology)

   Glass, Jennifer B. (Ed.)

   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. 

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4. Uncovering novel functions of the enigmatic, abundant, and active Anaerolineae in a salt marsh ecosystem

   https://doi.org/10.1128/msystems.01162-24  

   Payne, Paige E; Knobbe, Loren N; Chanton, Patricia; Zaugg, Julian; Mortazavi, Behzad; Mason, Olivia U (January 2025, 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. 

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5. Spatial evidence of cryptic methane cycling and methylotrophic metabolisms along a land–ocean transect in salt marsh sediment

   https://doi.org/10.1016/j.gca.2025.07.019  

   Krause, Sebastian JE; Wipfler, Rebecca; Liu, Jiarui; Yousavich, David J; Robinson, DeMarcus; Hoyt, David W; Orphan, Victoria J; Treude, Tina (September 2025, Geochimica et Cosmochimica Acta)

   Methylotrophic methanogenesis in the sulfate-rich zone of coastal and marine sediments couples with anaerobic oxidation of methane (AOM), forming the cryptic methane cycle. This study provides evidence of cryptic methane cycling in the sulfate-rich zone across a land–ocean transect of four stations–two brackish, one marine, and one hypersaline–within the Carpinteria Salt Marsh Reserve (CSMR), southern California, USA. Samples from the top 20 cm of sediment from the transect were analyzed through geochemical and molecular (16S rRNA) techniques, in-vitro methanogenesis incubations, and radiotracer incubations utilizing 35S-SO4, 14C-mono-methylamine, and 14C-CH4. Sediment methane concentrations were consistently low (3 to 28 µM) at all stations, except for the marine station, where methane increased with depth reaching 665 µM. Methanogenesis from mono-methylamine was detected throughout the sediment at all stations with estimated CH4 production rates in the sub-nanomolar to nanomolar range per cm3 sediment and day. 16S rRNA analysis identified methanogenic archaea (Methanosarcinaceae, Methanomassiliicoccales, and Methanonatronarchaeacea) capable of producing methane from methylamines in sediment where methylotrophic methanogenesis was found to be active. Metabolomic analysis of porewater showed mono-methylamine was mostly undetectable (<3 µM) or present in trace amounts (<10 µM) suggesting rapid metabolic turnover. In-vitro methanogenesis incubations of natural sediment showed no linear methane buildup, suggesting a process limiting methane emissions. AOM activity, measured with 14C-CH4, overlapped with methanogenesis from mono-methylamine activity at all stations, with rates ranging from 0.03 to 19.4 nmol cm− 3 d− 1. Geochemical porewater analysis showed the CSMR sediments are rich in sulfate and iron. Porewater sulfate concentrations (9–91 mM) were non-limiting across the transect, supporting sulfate reduction activity (1.5–2,506 nmol cm− 3 d− 1). Porewater sulfide and iron (II) profiles indicated that the sediment transitioned from a predominantly iron-reducing environment at the two brackish stations to a predominantly sulfate-reducing environment at the marine and hypersaline stations, which coincided with the presence of phyla (Desulfobacterota) involved in these processes. AOM activity overlapped with sulfate reduction and porewater iron (II) concentrations suggesting that AOM is likely coupled to sulfate and possibly iron reduction at all stations. However, 16S rRNA analysis identified anaerobic methanotrophs (ANME-2) only at the marine and hypersaline stations while putative methanogens were found in sediment across all stations. In one sediment horizon at the marine station, methanogen families (Methanosarcinaceae, Methanosaetaceae, Methanomassiliicoccales, and Methanoregulaceae) and ANME 2a,2b, and 2c groups were found together. Collectively, our data suggest that at the brackish stations methanogens alone may be involved in cryptic methane cycling, while at the marine and hypersaline stations both groups may be involved in the process. Differences in rate constants from incubations with 14C-labeled methane and mono-methylamine suggest a non-methanogenic process oxidizing mono-methylamine to inorganic carbon, likely mediated by sulfate-reducing bacteria. Understanding the potential competition of sulfate reducers with methanogens for mono-methylamine needs further investigation as it might be another important process responsible for low methane emissions in salt marshes. 

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