scholarly journals Streptomycesvolatile compounds influence exploration and microbial community dynamics by altering iron availability

2018 ◽  
Author(s):  
Stephanie E. Jones ◽  
Christine A. Pham ◽  
Joseph McKillip ◽  
Matthew Zambri ◽  
Erin E. Carlson ◽  
...  

ABSTRACTBacteria and fungi produce a wide array of volatile organic compounds (VOCs), and these can act as infochemicals or as competitive tools. Recent work has shown that the VOC trimethylamine (TMA) can promote a new form ofStreptomycesgrowth, termed ‘exploration’. Here, we report that TMA also serves to alter nutrient availability in the area surrounding exploring cultures: TMA dramatically increases the environmental pH, and in doing so, reduces iron availability. This, in turn, compromised the growth of other soil bacteria and fungi. In contrast,Streptomycesthrives in these iron-depleted niches by secreting a suite of differentially modified siderophores, and by upregulating genes associated with siderophore uptake. Further reducing iron levels by siderophore piracy, limiting siderophore uptake, or growing cultures in the presence of iron chelators, unexpectedly enhanced exploration. Our work reveals a new role for VOCs in modulating iron levels in the environment, and implies a critical role for VOCs in modulating the behaviour of microbes and the makeup of their communities.

mBio ◽  
2019 ◽  
Vol 10 (2) ◽  
Author(s):  
Stephanie E. Jones ◽  
Christine A. Pham ◽  
Matthew P. Zambri ◽  
Joseph McKillip ◽  
Erin E. Carlson ◽  
...  

ABSTRACTBacteria and fungi produce a wide array of volatile organic compounds (VOCs), and these can act as chemical cues or as competitive tools. Recent work has shown that the VOC trimethylamine (TMA) can promote a new form ofStreptomycesgrowth, termed “exploration.” Here, we report that TMA also serves to alter nutrient availability in the area surrounding exploring cultures: TMA dramatically increases the environmental pH and, in doing so, reduces iron availability. This, in turn, compromises the growth of other soil bacteria and fungi. In response to this low-iron environment,Streptomyces venezuelaesecretes a suite of differentially modified siderophores and upregulates genes associated with siderophore uptake. Further reducing iron levels by limiting siderophore uptake or growing cultures in the presence of iron chelators enhanced exploration. Exploration was also increased whenS. venezuelaewas grown in association with the related low-iron- and TMA-tolerantAmycolatopsisbacteria, due to competition for available iron. We are only beginning to appreciate the role of VOCs in natural communities. This work reveals a new role for VOCs in modulating iron levels in the environment and implies a critical role for VOCs in modulating the behavior of microbes and the makeup of their communities. It further adds a new dimension to our understanding of the interspecies interactions that influenceStreptomycesexploration and highlights the importance of iron in exploration modulation.IMPORTANCEMicrobial growth and community interactions are influenced by a multitude of factors. A new mode ofStreptomycesgrowth—exploration—is promoted by interactions with the yeastSaccharomycescerevisiaeand requires the emission of trimethylamine (TMA), a pH-raising volatile compound. We show here that TMA emission also profoundly alters the environment around exploring cultures. It specifically reduces iron availability, and this in turn adversely affects the viability of surrounding microbes. Paradoxically,Streptomycesbacteria thrive in these iron-depleted niches, both rewiring their gene expression and metabolism to facilitate iron uptake and increasing their exploration rate. Growth in close proximity to other microbes adept at iron uptake also enhances exploration. Collectively, the data from this work reveal a new role for bacterial volatile compounds in modulating nutrient availability and microbial community behavior. The results further expand the repertoire of interspecies interactions and nutrient cues that impactStreptomycesexploration and provide new mechanistic insight into this unique mode of bacterial growth.


2020 ◽  
Author(s):  
Ella T. Sieradzki ◽  
Erin E. Nuccio ◽  
Jennifer Pett-Ridge ◽  
Mary K. Firestone

AbstractNitrogen is a common limiting nutrient in soil in part because most N is present as macromolecular organic compounds, not directly available to plants. The microbial community present in soil near roots (rhizosphere) is in many ways analogous to the human gut microbiome, transforming nutrients present in organic substrates to forms available to plants through extracellular enzymes. Many recent studies have focused on the genetic potential for nitrogen cycling by bacteria in the rhizosphere, and on measuring inorganic N pools and fluxes. Between those two bodies of knowledge, there is scarce information on functionality of macromolecular nitrogen decomposing bacteria and fungi and how it relates to life stages of the plant. This is particularly important as many soil bacteria identified in community composition studies can be inactive or not viable. Here we use a time-series of metatranscriptomes from rhizosphere and bulk soil bacteria and fungi to follow extracellular protease and chitinase expression during rhizosphere aging. In addition, we explore the effect of adding plant litter as a source of macromolecular carbon and nitrogen. Expression of extracellular proteases increased over time in the absence of litter, more so in the presence of roots, whereas the dominant chitinase (chit1) was upregulated with exposure to litter. Structural groups of proteases were surprisingly dominated by serineproteases, possibly due to the importance of betaproteobacteria and actinobacteria in this grassland soil. Extracellular proteases of betaprotebacterial origin were more highly expressed in the presence of roots, whereas deltaroteobacteria and fungi responded to the presence of litter. We found functional guilds specializing in decomposition of proteins in the rhizosphere, detritusphere and in the vicinity of aging roots. We also identify a guild that appears to specialize in protein decomposition in the presence of roots and litter and increases its activity in aging rhizosphere, which may imply that this guild targets rhizodeposits or the senescing root itself as a protein source. Different temporal patterns of guilds imply that rather than functional redundancy, microbial decomposers operate within distinct niches.


2014 ◽  
Vol 281 (1795) ◽  
pp. 20140882 ◽  
Author(s):  
James A. Bradley ◽  
Joy S. Singarayer ◽  
Alexandre M. Anesio

Retreating ice fronts (as a result of a warming climate) expose large expanses of deglaciated forefield, which become colonized by microbes and plants. There has been increasing interest in characterizing the biogeochemical development of these ecosystems using a chronosequence approach. Prior to the establishment of plants, microbes use autochthonously produced and allochthonously delivered nutrients for growth. The microbial community composition is largely made up of heterotrophic microbes (both bacteria and fungi), autotrophic microbes and nitrogen-fixing diazotrophs. Microbial activity is thought to be responsible for the initial build-up of labile nutrient pools, facilitating the growth of higher order plant life in developed soils. However, it is unclear to what extent these ecosystems rely on external sources of nutrients such as ancient carbon pools and periodic nitrogen deposition. Furthermore, the seasonal variation of chronosequence dynamics and the effect of winter are largely unexplored. Modelling this ecosystem will provide a quantitative evaluation of the key processes and could guide the focus of future research. Year-round datasets combined with novel metagenomic techniques will help answer some of the pressing questions in this relatively new but rapidly expanding field, which is of growing interest in the context of future large-scale ice retreat.


Plants ◽  
2021 ◽  
Vol 10 (12) ◽  
pp. 2580
Author(s):  
Yi Zhang ◽  
Yingzhong Xie ◽  
Hongbin Ma ◽  
Juan Zhang ◽  
Le Jing ◽  
...  

Our study, which was conducted in the desert grassland of Ningxia in China (E 107.285, N 37.763), involved an experiment with five levels of annual precipitation 33% (R33), 66% (R66), 100% (CK), 133% (R133), 166% (R166) and two temperature levels (inside Open-Top Chamber (OTC) and outside OTC). Our objective was to determine how plant, soil bacteria, and fungi diversity respond to climate change. Our study suggested that plant α-diversity in CK and TCK were significantly higher than that of other treatments. Increased precipitation promoted root biomass (RB) growth more than aboveground living biomass (ALB). R166 promoted the biomass of Agropyron mongolicum the most. In the fungi communities, temperature and precipitation interaction promoted α-diversity. In the fungi communities, the combination of increased temperature and natural precipitation (TCK) promoted β-diversity the most, whose distance was determined to be 25,124 according to PCA. In the bacteria communities, β-diversity in CK was significantly higher than in other treatments, and the distance was determined to be 3010 according to PCA. Soil bacteria and fungi α- and β-diversity, and ALB promoted plant diversity the most. The interactive effects of temperature and precipitation on C, N, and P contents of plants were larger than their independent effects.


2019 ◽  
Author(s):  
Dima Chen ◽  
Ying Wu ◽  
Muhammad Saleem ◽  
Bing Wang ◽  
Shuijin Hu ◽  
...  

Abstract Soil harbors highly diverse abundant and rare microbial phylotypes that drive multiple soil functions. Given increasing intensity and frequency of vegetation loss and anthropogenic reactive nitrogen (N) inputs to the soil in the future, we lack a mechanistic understanding of how vegetation loss may influence abundant and rare microbial phylotypes at various N-enrichment levels. In the current study, we assessed the effects of vegetation loss on abundant and rare phylotypes of soil bacteria and fungi across three N-enrichment levels in a semi-arid grassland ecosystem. After six years of experimentation in with and without vegetation plots, the vegetation loss increased the total relative abundance of abundant soil bacterial phylotypes but not that of abundant fungal phylotypes at across N-enrichment levels. It is very likely because the number of abundant bacterial phylotypes with positive than negative responses to vegetation loss was higher; however, the number of abundant fungal phylotypes with positive than negative responses to vegetation loss was similar during this period. Moreover, the vegetation loss did not alter the alpha-diversity of abundant or rare bacterial phylotypes, or, of abundant fungal phylotypes; however, it reduced the alpha-diversity of rare fungal phylotypes at across N-enrichment levels. The vegetation loss, however, altered the beta-diversity of abundant and rare bacterial and fungal phylotypes across N-enrichment levels. We found that, against expectations, the effects of vegetation loss on the diversity of abundant and rare phylotypes of both bacteria and fungi were relatively consistent across N-enrichment levels. Our findings provide, for the first time, the phylotype-based data on how vegetation loss affects abundant and rare phylotypes of soil bacteria and fungi across N-enrichment levels. The results also indicate that the effects of vegetation loss on belowground functions may be relatively insensitive to the differences in the N-deposition rates.


2015 ◽  
Vol 168 ◽  
pp. 222-235 ◽  
Author(s):  
Eric H. Oelkers ◽  
Liane G. Benning ◽  
Stefanie Lutz ◽  
Vasileios Mavromatis ◽  
Christopher R. Pearce ◽  
...  

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