While interactions between roots and microorganisms have been intensively studied, we know little about interactions among root-associated microbes. We used random matrix theory-based network analysis of 16S rRNA genes to identify bacterial networks associated with wild oat (Avena fatua) over two seasons in greenhouse microcosms. Rhizosphere networks were substantially more complex than those in surrounding soils, indicating the rhizosphere has a greater potential for interactions and niche-sharing. Network complexity increased as plants grew, even as diversity decreased, highlighting that community organisation is not captured by univariate diversity. Covariations were predominantly positive (> 80%), suggesting that extensive mutualistic interactions may occur among rhizosphere bacteria; we identified quorum-based signalling as one potential strategy. Putative keystone taxa often had low relative abundances, suggesting low-abundance taxa may significantly contribute to rhizosphere function. Network complexity, a previously undescribed property of the rhizosphere microbiome, appears to be a defining characteristic of this habitat.
It is well known that rhizosphere microbiomes differ from those of surrounding soil, and yet we know little about how these root-associated microbial communities change through the growing season and between seasons. We analyzed the response of soil bacteria to roots of the common annual grass Avena fatua over two growing seasons using high-throughput sequencing of 16S rRNA genes. Over the two periods of growth, the rhizosphere bacterial communities followed consistent successional patterns as plants grew, although the starting communities were distinct. Succession in the rhizosphere was characterized by a significant decrease in both taxonomic and phylogenetic diversity relative to background soil communities, driven by reductions in both richness and evenness of the bacterial communities. Plant roots selectively stimulated the relative abundance of Alphaproteobacteria, Betaproteobacteria, and Bacteroidetes but reduced the abundance of Acidobacteria, Actinobacteria, and Firmicutes. Taxa that increased in relative abundance in the rhizosphere soil displayed phylogenetic clustering, suggesting some conservation and an evolutionary basis for the response of complex soil bacterial communities to the presence of plant roots. The reproducibility of rhizosphere succession and the apparent phylogenetic conservation of rhizosphere competence traits suggest adaptation of the indigenous bacterial community to this common grass over the many decades of its presence.
Arbuscular mycorrhizal fungi (AMF) perform an important ecosystem service by improving plant nutrient capture from soil, yet little is known about how AMF influence soil microbial communities during nutrient uptake. We tested whether an AMF modifies the soil microbial community and nitrogen cycling during litter decomposition. A two-chamber microcosm system was employed to create a root-free soil environment to control AMF access to (13) C- and (15) N-labelled root litter. Using a 16S rRNA gene microarray, we documented that approximately 10% of the bacterial community responded to the AMF, Glomus hoi. Taxa from the Firmicutes responded positively to AMF, while taxa from the Actinobacteria and Comamonadaceae responded negatively to AMF. Phylogenetic analyses indicate that AMF may influence bacterial community assembly processes. Using nanometre-scale secondary ion mass spectrometry (NanoSIMS) we visualized the location of AMF-transported (13) C and (15) N in plant roots. Bulk isotope ratio mass spectrometry revealed that the AMF exported 4.9% of the litter (15) N to the host plant (Plantago lanceolata L.), and litter-derived (15) N was preferentially exported relative to litter-derived (13) C. Our results suggest that the AMF primarily took up N in the inorganic form, and N export is one mechanism by which AMF could modify the soil microbial community and decomposition processes.
We investigated arbuscular mycorrhizal fungi (AMF) alteration of microbial mediation of litter decomposition. AMF (Glomus hoi) were either allowed access to or excluded from Plantago lanceolata L. root litter embedded in soil; litter was labeled with either (13) C only or (13) C and (15) N. Plant N uptake was significantly increased if AMF accessed the litter, and (15) N analysis of the plant material indicated that 2-3% of plant N originated from litter. Succession of the soil community mediating decomposition was assessed by phospholipid fatty acids (PLFA) combined with (13) C-PLFA. During the first 21 days of decomposition, saprotrophic fungi and Gram-negative bacteria were the dominant consumers of litter C. As decomposition progressed however, (13) C content of the fungal biomarkers declined substantially, and Gram-negative and Gram-positive bacteria became the primary reservoirs of labeled litter C. The putative PLFA marker for AMF (16:1ω5c) originated primarily from non-AMF sources. In AMF-invaded root litter, Gram-negative, Gram-positive, and 16:1ω5c markers became less (13) C-enriched relative to their counterparts in non-AMF-invaded microcosms during active decomposition. These patterns of (13) C: (12) C enrichment may result from AMF supply of (12) C from the plant to the decomposing soil microbial community; such C inputs could alter the microbial mediation of litter decomposition.
The rhizosphere is a hotspot for microbial C transformations, and the origin of root polysaccharides and polymeric carbohydrates that are important precursors to soil organic matter. However, the ecological mechanisms that underpin rhizosphere carbohydrate depolymerization are poorly understood. Using Avena fatua, a common annual grass, we analyzed time-resolved metatranscriptomes to compare microbial function in rhizosphere, detritusphere, and combined rhizosphere-detritusphere habitats. Population transcripts were binned with a unique reference database generated from soil isolate and single amplified genomes, metagenomes, and stable isotope probing metagenomes. While soil habitat significantly affected both community composition and overall gene expression, succession of microbial functions occurred at a faster time scale than compositional changes. Using hierarchical clustering of upregulated decomposition gene expression, we identified four distinct microbial guilds populated by taxa whose functional succession patterns suggest specialization for substrates provided by fresh growing roots, decaying root detritus, the combination of live and decaying root biomass, or aging root material. Carbohydrate depolymerization genes were consistently upregulated in the rhizosphere, and both taxonomic and functional diversity were high in the combined rhizosphere-detritusphere-suggesting coexistence of rhizosphere guilds is facilitated by niche differentiation. Metatranscriptome-defined guilds provide a framework to model rhizosphere succession and its consequences for soil carbon cycling. .
Viruses impact nearly all organisms on Earth, with ripples of influence in agriculture, health, and biogeochemical processes. However, very little is known about RNA viruses in an environmental context, and even less is known about their diversity and ecology in soil, 1 of the most complex microbial systems. Here, we assembled 48 individual metatranscriptomes from 4 habitats within a planted soil sampled over a 22-d time series: Rhizosphere alone, detritosphere alone, rhizosphere with added root detritus, and unamended soil (4 time points and 3 biological replicates). We resolved the RNA viral community, uncovering a high diversity of viral sequences. We also investigated possible host organisms by analyzing metatranscriptome marker genes. Based on viral phylogeny, much of the diversity wasNarnaviridaethat may parasitize fungi orLeviviridae, which may infect Proteobacteria. Both host and viral communities appear to be highly dynamic, and rapidly diverged depending on experimental conditions. The viral and host communities were structured based on the presence of root litter. Clear temporal dynamics byLeviviridaeand their hosts indicated that viruses were replicating. With this time-resolved analysis, we show that RNA viruses are diverse, abundant, and active in soil. When viral infection causes host cell death, it may mobilize cell carbon in a process that may represent an overlooked component of soil carbon cycling.
Viruses impact nearly all organisms on Earth, with ripples of influence in agriculture, health and biogeochemical processes. However, very little is known about RNA viruses in an environmental context, and even less is known about their diversity and ecology in the most complex microbial system, soil. Here, we assembled 48 individual metatranscriptomes from four habitats within a soil sampled over a 22-day time series: rhizosphere alone, detritosphere alone, a combination of the two, and unamended soil (four time points and three biological replicates per time point). We resolved the RNA viral community, uncovering a high diversity of viral sequences. We also investigated possible host organisms by analyzing metatranscriptome marker gene content. Based on viral phylogeny, much of the diversity was Narnaviridae that parasitize fungi or Leviviridae that infect Proteobacteria. Both host and viral communities appear to be highly dynamic, and rapidly diverged depending on experimental conditions. The viral communities were structured based on the presence of litter, while putative hosts appeared to be impacted by both the presence of litter and roots. A clear time signature from Leviviridae and their hosts indicated that viruses were replicating. With this time-resolved analysis, we show that RNA viruses are diverse, abundant and active in soil. Their replication causes host cell death, mobilizing carbon in a process that represents a largely overlooked component of carbon cycling in soil.
Microbial activity increases after rewetting dry soil, resulting in a pulse of carbon mineralization and nutrient availability. The biogeochemical responses to wet-up are reasonably well understood and known to be microbially mediated. Yet, the population level dynamics, and the resulting changes in microbial community patterns, are not well understood as ecological phenomena. Here, we used sequencing of 16S rRNA genes coupled with heavy water (H 2 18 O) DNA quantitative stable isotope probing to estimate population-specific rates of growth and mortality in response to a simulated wet-up event in a California annual grassland soil. Bacterial growth and mortality responded rapidly to wet-up, within 3 h, and continued throughout the 168 h incubation, with patterns of sequential growth observed at the phylum level. Of the 37 phyla detected in the prewet community, growth was found in 18 phyla while mortality was measured in 26 phyla. Rapid growth and mortality rates were measurable within 3 h of wet-up but had contrasting characteristics; growth at 3 h was dominated by select taxa within the Proteobacteria and Firmicutes, whereas mortality was taxonomically widespread. Furthermore, across the community, mortality exhibited density-independence, consistent with the indiscriminate shock resulting from dry-down and wet-up, whereas growth was density-dependent, consistent with control by competition or predation. Total aggregated growth across the community was highly correlated with total soil CO 2 production. Together, these results illustrate how previously "invisible" population responses can translate quantitatively to emergent observations of ecosystem-scale biogeochemistry.
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