scholarly journals StreptomycesVolatile Compounds Influence Exploration and Microbial Community Dynamics by Altering Iron Availability

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.

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.


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.


2020 ◽  
Vol 2 (7A) ◽  
Author(s):  
Frederik De Boever ◽  
Philippe Potin ◽  
David Green

A major challenge in microbial ecology is to understand the stability of interspecies interactions when progressing from pairs of interacting species to multispecies interaction networks. A lack of direct evidence, and a conceptual framework to explore how direct and indirect effects shape cellular responses in species-rich networks has hindered progress in our understanding of these combined effects. Here we aimed to investigate whether higher-order interactions shape community dynamics and transcriptional profiles of all interacting partners in a simplified microbial community that includes a primary producer (Nannochloropsis oceanica CCAP849/10) and two heterotrophic bacteria (Marinobacter sp. FDB33 and Alteromonas sp. FDB36). By combining co-cultivation assays, quantification of absolute abundances, nutrient analysis, and simultaneous RNA-sequencing, we reveal genome-wide transcriptional responses in all binary co-cultivation partners and show that the third partner can profoundly alter binary interactions at the phenotypic and transcription level. Our study demonstrates the context-dependency of binary interactions, whereby environmental conditions and the presence of specific organisms can affect the cellular physiology of the interacting partners and ultimately the stability of the community. Furthermore, our approach provides a powerful tool for probing the molecular basis of emergent properties in more complex systems.


2015 ◽  
Vol 81 (7) ◽  
pp. 2525-2533 ◽  
Author(s):  
Daniel J. O'Sullivan ◽  
Paul D. Cotter ◽  
Orla O'Sullivan ◽  
Linda Giblin ◽  
Paul L. H. McSweeney ◽  
...  

ABSTRACTWe sought to determine if the time, within a production day, that a cheese is manufactured has an influence on the microbial community present within that cheese. To facilitate this, 16S rRNA amplicon sequencing was used to elucidate the microbial community dynamics of brine-salted continental-type cheese in cheeses produced early and late in the production day. Differences in the microbial composition of the core and rind of the cheese were also investigated. Throughout ripening, it was apparent that cheeses produced late in the day had a more diverse microbial population than their early equivalents. Spatial variation between the cheese core and rind was also noted in that cheese rinds were initially found to have a more diverse microbial population but thereafter the opposite was the case. Interestingly, the generaThermus,Pseudoalteromonas, andBifidobacterium, not routinely associated with a continental-type cheese produced from pasteurized milk, were detected. The significance, if any, of the presence of these genera will require further attention. Ultimately, the use of high-throughput sequencing has facilitated a novel and detailed analysis of the temporal and spatial distribution of microbes in this complex cheese system and established that the period during a production cycle at which a cheese is manufactured can influence its microbial composition.


mSystems ◽  
2020 ◽  
Vol 5 (6) ◽  
pp. e00493-20
Author(s):  
John L. Chodkowski ◽  
Ashley Shade

ABSTRACTMicrobial exponential growth is expected to occur infrequently in environments that have long periods of nutrient starvation punctuated by short periods of high nutrient flux. These conditions likely impose nongrowth states for microbes. However, nongrowth states are uncharacterized for the majority of environmental bacteria, especially in regard to exometabolite production. We compared exometabolites produced over stationary phase across three environmental bacteria: Burkholderia thailandensis E264 (ATCC 700388), Chromobacterium violaceum ATCC 31532, and Pseudomonas syringae pv. tomato DC3000 (ATCC BAA-871). We grew each strain in monoculture and investigated exometabolite dynamics from mid-exponential to stationary phases. We focused on exometabolites that were released into the medium and accumulated over 45 h, including approximately 20 h of stationary phase. We also analyzed transcripts (transcriptome sequencing [RNA-seq]) to interpret exometabolite output. We found that the majority of exometabolites released were strain specific, with a subset of identified exometabolites involved in both central and secondary metabolism. Transcript analysis supported that exometabolites were released from intact cells, as various transporters had either increased or consistent transcripts through time. Interestingly, we found that succinate was one of the most abundant identifiable exometabolites for all strains and that each strain rerouted their metabolic pathways involved in succinate production during stationary phase. These results show that nongrowth states can be metabolically dynamic and that environmental bacteria can enrich a minimal environment with diverse chemical compounds as a consequence of growth and postgrowth maintenance in stationary phase. This work provides insights into microbial community interactions via exometabolites under conditions of growth cessation or limitation.IMPORTANCE Nongrowth states are common for bacteria that live in environments that are densely populated and predominantly nutrient exhausted, and yet these states remain largely uncharacterized in cellular metabolism and metabolite output. Here, we investigated and compared stationary-phase exometabolites and RNA transcripts for each of three environmental bacterial strains. We observed that diverse exometabolites were produced and provide evidence that these exometabolites accumulate over time through release by intact cells. Additionally, each bacterial strain had a characteristic exometabolite profile and exhibited dynamics in exometabolite composition. This work affirms that stationary phase is metabolically dynamic, with each strain tested creating a unique chemical signature in the extracellular space and altering metabolism in stationary phase. These findings set the stage for understanding how bacterial populations can support surrounding neighbors in environments with prolonged nutrient exhaustion through exometabolite-mediated interspecies interactions.


2020 ◽  
Vol 13 (10) ◽  
pp. 275
Author(s):  
Ravneet Chhabra ◽  
Aishwarya Saha ◽  
Ashkon Chamani ◽  
Nicole Schneider ◽  
Riya Shah ◽  
...  

Iron is an essential element required to support the health of organisms. This element is critical for regulating the activities of cellular enzymes including those involved in cellular metabolism and DNA replication. Mechanisms that underlie the tight control of iron levels are crucial in mediating the interaction between microorganisms and their host and hence, the spread of infection. Microorganisms including viruses, bacteria, and fungi have differing iron acquisition/utilization mechanisms to support their ability to acquire/use iron (e.g., from free iron and heme). These pathways of iron uptake are associated with promoting their growth and virulence and consequently, their pathogenicity. Thus, controlling microorganismal survival by limiting iron availability may prove feasible through the use of agents targeting their iron uptake pathways and/or use of iron chelators as a means to hinder development of infections. This review will serve to assimilate findings regarding iron and the pathogenicity of specific microorganisms, and furthermore, find whether treating infections mediated by such organisms via iron chelation approaches may have potential clinical benefit.


2015 ◽  
Vol 6 ◽  
Author(s):  
Fatma A. A. Aziz ◽  
Kenshi Suzuki ◽  
Akihiro Ohtaki ◽  
Keita Sagegami ◽  
Hidetaka Hirai ◽  
...  

2018 ◽  
Vol 84 (16) ◽  
Author(s):  
Carla E. Rosenfeld ◽  
Bruce R. James ◽  
Cara M. Santelli

ABSTRACTMining and other industrial activities worldwide have resulted in Se-enriched surface soils, which pose risks to human and environmental health. Although not well studied, microbial activity can alter Se bioavailability and distribution, even in oxic environments. We used high-throughput sequencing to profile bacterial and fungal communities inhabiting mine soils in southeastern Idaho, comparing mined and unmined locations within two reclaimed phosphate mine areas containing various Se concentrations. The goal was to determine whether microbial communities differed in (i) different mines, (ii) mined areas compared to unmined areas, and (iii) various soil Se concentrations. Though reclamation occurred 20 to 30 years ago, microbial community structures in mined soils were significantly altered compared to unmined soils, suggesting persistent mining-related impacts on soil processes. Additionally, operational taxonomic unit with a 97% sequence similarity cutoff (OTU0.03) richness and diversity were significantly diminished with increasing Se, though not with other geochemical parameters, suggesting that Se contamination shapes communities in favor of Se-tolerant microorganisms. Two bacterial phyla,ActinobacteriaandGemmatimonadetes, were enriched in high-Se soils, while for fungi, Ascomycota dominated all soils regardless of Se concentration. Combining diversity analyses and taxonomic patterns enables us to move toward connecting physiological function of microbial groups to Se biogeochemical cycling in oxic soil environments.IMPORTANCESelenium contamination in natural environments is of great concern globally, and microbial processes are known to mediate Se transformations. Such transformations alter Se mobility, bioavailability, and toxicity, which can amplify or mitigate Se pollution. To date, nearly all studies investigating Se-microbe interactions have used culture-based approaches with anaerobic bacteria despite growing knowledge that (i) aerobic Se transformations can occur, (ii) such transformations can be mediated by microorganisms other than bacteria, and (iii) microbial community dynamics, rather than individual organismal activities, are important for metal(loid) cycling in natural environments. We examined bacterial and fungal communities in Se-contaminated reclaimed mine soils and found significant declines in diversity at high Se concentrations. Additionally, we identified specific taxonomic groups that tolerate excess Se and may be useful for bioremediation purposes. These patterns were similar across mines of different ages, suggesting that microbial community impacts may persist long after physicochemical parameters indicate complete site recovery.


mBio ◽  
2016 ◽  
Vol 7 (3) ◽  
Author(s):  
Catherine R. Armbruster ◽  
Daniel J. Wolter ◽  
Meenu Mishra ◽  
Hillary S. Hayden ◽  
Matthew C. Radey ◽  
...  

ABSTRACTWhile considerable research has focused on the properties of individual bacteria, relatively little is known about how microbial interspecies interactions alter bacterial behaviors and pathogenesis.Staphylococcus aureusfrequently coinfects with other pathogens in a range of different infectious diseases. For example, coinfection byS. aureuswithPseudomonas aeruginosaoccurs commonly in people with cystic fibrosis and is associated with higher lung disease morbidity and mortality.S. aureussecretes numerous exoproducts that are known to interact with host tissues, influencing inflammatory responses. The abundantly secretedS. aureusstaphylococcal protein A (SpA) binds a range of human glycoproteins, immunoglobulins, and other molecules, with diverse effects on the host, including inhibition of phagocytosis ofS. aureuscells. However, the potential effects of SpA and otherS. aureusexoproducts on coinfecting bacteria have not been explored. Here, we show thatS. aureus-secreted products, including SpA, significantly alter two behaviors associated with persistent infection. We found that SpA inhibited biofilm formation by specificP. aeruginosaclinical isolates, and it also inhibited phagocytosis by neutrophils of all isolates tested. Our results indicate that these effects were mediated by binding to at least twoP. aeruginosacell surface structures—type IV pili and the exopolysaccharide Psl—that confer attachment to surfaces and to other bacterial cells. Thus, we found that the role of a well-studiedS. aureusexoproduct, SpA, extends well beyond interactions with the host immune system. Secreted SpA alters multiple persistence-associated behaviors of another common microbial community member, likely influencing cocolonization and coinfection with other microbes.IMPORTANCEBacteria rarely exist in isolation, whether on human tissues or in the environment, and they frequently coinfect with other microbes. However, relatively little is known about how microbial interspecies interactions alter bacterial behaviors and pathogenesis. We identified a novel interaction between two bacterial species that frequently infect together—Staphylococcus aureusandPseudomonas aeruginosa. We show that theS. aureus-secreted protein staphylococcal protein A (SpA), which is well-known for interacting with host targets, also binds to specificP. aeruginosacell surface molecules and alters two persistence-associatedP. aeruginosabehaviors: biofilm formation and uptake by host immune cells. BecauseS. aureusfrequently precedesP. aeruginosain chronic infections, these findings reveal how microbial community interactions can impact persistence and host interactions during coinfections.


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