Sonic Species Relativ - Micro Music (Dominant Space Remix)
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Overall, at the phylum level, prokaryotic communities were predominated by ASVs from the Proteobacteria (46.7%), Chloroflexi (15.2%), Bacteroidetes (8.4), Epsilonbacteraeota (3.7%), Spirochaetes (3.6%), and Acidobacteria (3.5%) phyla (Fig. S6). At higher S. alterniflora biomass, an increase in the relative abundance of Proteobacteria ASVs and a decline in the relative abundance of Chloroflexi and Spirochaetes ASVs was observed (Fig. S6). At increasing proximity from the root, the relative abundance of Proteobacteria, Spirochaetes, and Epsilonbacteraeota increased while Acidobacteria and Bacteroidetes decreased (Fig. S6). Prokaryotic taxa with the potential to catalyze redox reactions in the S, Fe, and N cycles were investigated in greater detail due to their known significance in salt marsh ecosystem functioning. Putative function was inferred based on homology at the genus level with described prokaryotic species (Table S1). Prokaryotes putatively capable of nitrification (a.k.a. nitrifiers) exhibited higher relative abundance in areas colonized by the tall S. alterniflora phenotype, in comparison to areas occupied by the short and medium phenotypes (Fig. 4a). Dominant nitrifiers in the studied system included members of the bacterial genera Candidatus Nitrotoga and Nitrospira, as well as the archaeal genus Candidatus Nitrosopumilus (Fig. 4a). Additionally, a significant enrichment in taxa potentially involved in the Fe and S cycles was detected in the plant root relative to the bulk sediment (Fig. 4b, c, d). The putative Fe oxidizer of the Zetaproteobacteria, Mariprofundus sp., showed high relative abundance in the roots of the tall S. alterniflora phenotype, while Acidihalobacter of the Gammaproteobacteria was the predominant Fe oxidizer in the roots of the short phenotype (Fig. 4b). Putative autotrophic endosymbionts capable of S oxidation from the Candidatus Thiodiazotropha genus and Thiomicrospirales order preferably colonized the roots of S. alterniflora regardless of plant phenotype (Fig. 4c). Sulfur oxidizers from the Sulfurovum genus preferentially colonized the areas dominated by the short S. alterniflora phenotype in all compartments (Fig. 4c). Putative sulfate reducers of the Desulfobacterales order: Desulfatitalea, Desulfopila, and Desulfosarcina genera were enriched at closer proximities to the S. alterniflora root (Fig. 4d).
Although sulfide is generally considered as a potent phytotoxin, moderately sulfidic conditions (< 1 mM) have been shown to actually stimulate S. alterniflora growth in a controlled laboratory experiment [71]. Energy conservation from sulfide oxidation in the root tissue was speculated to be the driver of increased plant primary production [68]. Furthermore, sulfide oxidation to sulfate has been demonstrated inside S. alterniflora root tissues using isotope tracers [11, 50]. However, it is still not clear what process, biological or chemical, dominates sulfide oxidation inside S. alterniflora roots. We propose that S. alterniflora shares a symbiotic relationship with S oxidizers in both the rhizosphere and root compartments. Sulfur oxidation may be mediated by not only Candidatus Thiodiazotropha bacteria, but also members of the Sulfurovum and Thioalkalispira genera or endosymbionts from the Thiomicrospirales order. Previously studied microbial species from the Sulfurovum genus and endosymbionts from the Thiomicrospirales order have been demonstrated to fix C; whereas members from Desulfovibrio, Thioalkalispira, and Candidatus Thiodiazotropha genera have been shown to perform both C and N fixation [4, 75, 89, 91]. Moreover, Crump et al. [14] studying the root microbiome of seagrass Zostera spp. found high transcript levels of N fixing and sulfur-oxidizing genes from Gammaproteobacteria species, including endosymbionts of marine invertebrates from the Sedimenticolaceae family, which includes the Candidatus Thiodiazotropha genus. Given that the S. alterniflora root zone is enriched in reduced S and its growth is limited by N uptake, we suggest that diazotrophy coupled to sulfide oxidation may be a key process that was previously overlooked. However, direct measurements of N and C fixation, and sulfur oxidation in the roots of S. alterniflora, their rates and controls, along with their relative contribution to plant growth remain unclear and require further research. Given that most studies, including this study, have inferred the coupling of S oxidation and N fixation based on gene homology and/or taxonomic placement, this interpretation should be treated with caution.
We studied a gradient in S. alterniflora productivity to characterize the ecology and physiology of the S. alterniflora root-associated microbiome and its potential role in shaping plant physiological performance. In sediments from the tall S. alterniflora phenotype, higher prokaryotic biomass and more rapid microbial mineralization of organic matter were linked to greater inorganic nutrient replenishment for plant uptake. Prokaryotic communities from bulk and rhizospheric sediment associated with the tall S. alterniflora phenotype contained the highest alpha diversity, while a decline in diversity was observed in the root in comparison to the bulk and rhizosphere sediment compartments in all S. alterniflora phenotypes. A marked decrease in prokaryotic alpha diversity with high abundances and increased phylogenetic dispersion was observed in the S. alterniflora root compartment. Thus, we propose that the S. alterniflora root microbiome is dominated by highly active and competitive species taking advantage of available carbon substrates in the oxidized root zone. The high relative abundance of prokaryotic ASVs with putative S oxidation and sulfate reduction capability in the S. alterniflora rhizosphere and root suggests a rapid S cycle at close proximity to, or even inside, the root tissue. Moreover, both functional guilds were overrepresented in the S. alterniflora rhizosphere and root core microbiome. Rapid recycling of S is crucial for organic matter mineralization in anoxic marsh sediments. Thus, we propose that S. alterniflora shares a symbiotic relationship with S oxidizing bacteria in both the rhizosphere and root compartments. Sulfur oxidizers may benefit S. alterniflora plants not only by removing potentially toxic sulfide from the root zone, but also by coupling S oxidation with N and/or C fixation. The contribution to plant growth of each of these microbial processes represents a knowledge gap that warrants further research.
The S. alterniflora core root microbiome was investigated. For this study, an ASV prevalence threshold was operationally defined by plotting the relative abundance and richness of the rhizosphere and root core microbiomes at 10% intervals from 0 to 100% ASV prevalence cutoffs (Fig. S8). A conservative prevalence cutoff of 60% was determined by visually inspecting a threshold in which richness remained stable at increasing cutoff values (Fig. S8). Finally, putative nitrifying, S oxidizing, S/sulfate reducing, and Fe oxidizing function was inferred based on homology of ASVs at the genus level with previously described prokaryotic species (Table S1). 59ce067264
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