scholarly journals Lytic bacteriophage have diverse indirect effects in a synthetic cross-feeding community

2019 ◽  
Vol 14 (1) ◽  
pp. 123-134 ◽  
Author(s):  
Lisa Fazzino ◽  
Jeremy Anisman ◽  
Jeremy M. Chacón ◽  
Richard H. Heineman ◽  
William R. Harcombe

Abstract Bacteriophage shape the composition and function of microbial communities. Yet it remains difficult to predict the effect of phage on microbial interactions. Specifically, little is known about how phage influence mutualisms in networks of cross-feeding bacteria. We mathematically modeled the impacts of phage in a synthetic microbial community in which Escherichia coli and Salmonella enterica exchange essential metabolites. In this model, independent phage attack of either species was sufficient to temporarily inhibit both members of the mutualism; however, the evolution of phage resistance facilitated yields similar to those observed in the absence of phage. In laboratory experiments, attack of S. enterica with P22vir phage followed these modeling expectations of delayed community growth with little change in the final yield of bacteria. In contrast, when E. coli was attacked with T7 phage, S. enterica, the nonhost species, reached higher yields compared with no-phage controls. T7 infection increased nonhost yield by releasing consumable cell debris, and by driving evolution of partially resistant E. coli that secreted more carbon. Our results demonstrate that phage can have extensive indirect effects in microbial communities, that the nature of these indirect effects depends on metabolic and evolutionary mechanisms, and that knowing the degree of evolved resistance leads to qualitatively different predictions of bacterial community dynamics in response to phage attack.

2019 ◽  
Author(s):  
Lisa Fazzino ◽  
Jeremy Anisman ◽  
Jeremy M. Chacón ◽  
Richard H. Heineman ◽  
William R. Harcombe

AbstractBacteriophage shape the composition and function of microbial communities. Yet, it remains difficult to predict the effect of phage on microbial interactions. Specifically, little is known about how phage influence mutualisms in networks of cross-feeding bacteria. We modeled the impacts of phage in a synthetic microbial community in whichEscherichia coliandSalmonella entericaexchange essential metabolites. In this model, phage attack of either species was sufficient to inhibit both members of the mutualism; however, the evolution of phage resistance ultimately allowed both species to attain yields similar to those observed in the absence of phage. In laboratory experiments, attack ofS. entericawith P22virphage followed these modeling expectations of delayed community growth with little change in the final yield of bacteria. In contrast, whenE. coliwas attacked with T7 phage,S. enterica, the non-host species, reached higher yields compared to no-phage controls. T7 increased non-host yield by releasing consumable cell debris and by driving evolution of phage resistantE. colithat secreted more carbon. Additionally,E. colievolved only partial resistance, increasing the total amount of lysed cells available forS. entericato consume. Our results demonstrate that phage can have extensive indirect effects in microbial communities, and that the nature of these indirect effects depends on metabolic and evolutionary mechanisms.


2019 ◽  
Vol 2019 ◽  
pp. 1-5 ◽  
Author(s):  
Emanuele Bosi ◽  
Flavia Mascagni

Organisms change to adapt to the environment in which they live, evolving with coresiding individuals. Classic Darwinism postulates the primal importance of antagonistic interactions and selfishness as a major driver of evolution, promoting an increase of genomic and organism complexities. Recently, advancements in evolutionary ecology reshaped this notion, showing how leakiness in biological functions favours the adaptive genome reduction, leading to the emergence of codependence patterns. Microbial communities are complex entities exerting a gargantuan influence on the environment and the biology of the eukaryotic hosts they are associated with. Notwithstanding, we are still far from a comprehension of the ecological and evolutionary mechanisms governing the community dynamics. Here, we review the implications of genome streamlining into the unfolding of codependence within microbial communities and how this translates to an understanding of ecological patterns underlying the emerging properties of the community.


2018 ◽  
Author(s):  
Chenhao Li ◽  
Lisa Tucker-Kellogg ◽  
Niranjan Nagarajan

AbstractA growing body of literature points to the important roles that different microbial communities play in diverse natural environments and the human body. The dynamics of these communities is driven by a range of microbial interactions from symbiosis to predator-prey relationships, the majority of which are poorly understood, making it hard to predict the response of the community to different perturbations. With the increasing availability of high-throughput sequencing based community composition data, it is now conceivable to directly learn models that explicitly define microbial interactions and explain community dynamics. The applicability of these approaches is however affected by several experimental limitations, particularly the compositional nature of sequencing data. We present a new computational approach (BEEM) that addresses this key limitation in the inference of generalised Lotka-Volterra models (gLVMs) by coupling biomass estimation and model inference in an expectation maximization like algorithm (BEEM). Surprisingly, BEEM outperforms state-of-the-art methods for inferring gLVMs, while simultaneously eliminating the need for additional experimental biomass data as input. BEEM’s application to previously inaccessible public datasets (due to the lack of biomass data) allowed us for the first time to analyse microbial communities in the human gut on a per individual basis, revealing personalised dynamics and keystone species.


eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Manon Morin ◽  
Emily C Pierce ◽  
Rachel J Dutton

Microbial community structure and function rely on complex interactions whose underlying molecular mechanisms are poorly understood. To investigate these interactions in a simple microbiome, we introduced E. coli into an experimental community based on a cheese rind and identified the differences in E. coli’s genetic requirements for growth in interactive and non-interactive contexts using Random Barcode Transposon Sequencing (RB-TnSeq) and RNASeq. Genetic requirements varied among pairwise growth conditions and between pairwise and community conditions. Our analysis points to mechanisms by which growth conditions change as a result of increasing community complexity and suggests that growth within a community relies on a combination of pairwise and higher-order interactions. Our work provides a framework for using the model organism E. coli as a readout to investigate microbial interactions regardless of the genetic tractability of members of the studied ecosystem.


2020 ◽  
Vol 86 (13) ◽  
Author(s):  
Breah LaSarre ◽  
Adam M. Deutschbauer ◽  
Crystal E. Love ◽  
James B. McKinlay

ABSTRACT Microbial interactions abound in natural ecosystems and shape community structure and function. Substantial attention has been given to cataloging mechanisms by which microbes interact, but there is a limited understanding of the genetic landscapes that promote or hinder microbial interactions. We previously developed a mutualistic coculture pairing Escherichia coli and Rhodopseudomonas palustris, wherein E. coli provides carbon to R. palustris in the form of glucose fermentation products and R. palustris fixes N2 gas and provides nitrogen to E. coli in the form of NH4+. The stable coexistence and reproducible trends exhibited by this coculture make it ideal for interrogating the genetic underpinnings of a cross-feeding mutualism. Here, we used random barcode transposon sequencing (RB-TnSeq) to conduct a genome-wide search for E. coli genes that influence fitness during cooperative growth with R. palustris. RB-TnSeq revealed hundreds of genes that increased or decreased E. coli fitness in a mutualism-dependent manner. Some identified genes were involved in nitrogen sensing and assimilation, as expected given the coculture design. The other identified genes were involved in diverse cellular processes, including energy production and cell wall and membrane biogenesis. In addition, we discovered unexpected purine cross-feeding from R. palustris to E. coli, with coculture rescuing growth of an E. coli purine auxotroph. Our data provide insight into the genes and gene networks that can influence a cross-feeding mutualism and underscore that microbial interactions are not necessarily predictable a priori. IMPORTANCE Microbial communities impact life on Earth in profound ways, including driving global nutrient cycles and influencing human health and disease. These community functions depend on the interactions that resident microbes have with the environment and each other. Thus, identifying genes that influence these interactions will aid the management of natural communities and the use of microbial consortia as biotechnology. Here, we identified genes that influenced Escherichia coli fitness during cooperative growth with a mutualistic partner, Rhodopseudomonas palustris. Although this mutualism centers on the bidirectional exchange of essential carbon and nitrogen, E. coli fitness was positively and negatively affected by genes involved in diverse cellular processes. Furthermore, we discovered an unexpected purine cross-feeding interaction. These results contribute knowledge on the genetic foundation of a microbial cross-feeding interaction and highlight that unanticipated interactions can occur even within engineered microbial communities.


mSystems ◽  
2017 ◽  
Vol 2 (5) ◽  
Author(s):  
Valerie Hubalek ◽  
Moritz Buck ◽  
BoonFei Tan ◽  
Julia Foght ◽  
Annelie Wendeberg ◽  
...  

ABSTRACT Microbial interactions between Archaea and Bacteria mediate many important chemical transformations in the biosphere from degrading abundant polymers to synthesis of toxic compounds. Two of the most pressing issues in microbial interactions are how consortia are established and how we can modulate these microbial communities to express desirable functions. Here, we propose that public goods (i.e., metabolites of high energy demand in biosynthesis) facilitate energy conservation for life under energy-limited conditions and determine the assembly and function of the consortia. Our report suggests that an understanding of public good dynamics could result in new ways to improve microbial pollutant degradation in anaerobic systems. Syntrophy among Archaea and Bacteria facilitates the anaerobic degradation of organic compounds to CH4 and CO2. Particularly during aliphatic and aromatic hydrocarbon mineralization, as in the case of crude oil reservoirs and petroleum-contaminated sediments, metabolic interactions between obligate mutualistic microbial partners are of central importance. Using micromanipulation combined with shotgun metagenomic approaches, we describe the genomes of complex consortia within short-chain alkane-degrading cultures operating under methanogenic conditions. Metabolic reconstruction revealed that only a small fraction of genes in the metagenome-assembled genomes encode the capacity for fermentation of alkanes facilitated by energy conservation linked to H2 metabolism. Instead, the presence of inferred lifestyles based on scavenging anabolic products and intermediate fermentation products derived from detrital biomass was a common feature. Additionally, inferred auxotrophy for vitamins and amino acids suggests that the hydrocarbon-degrading microbial assemblages are structured and maintained by multiple interactions beyond the canonical H2-producing and syntrophic alkane degrader-methanogen partnership. Compared to previous work, our report points to a higher order of complexity in microbial consortia engaged in anaerobic hydrocarbon transformation. IMPORTANCE Microbial interactions between Archaea and Bacteria mediate many important chemical transformations in the biosphere from degrading abundant polymers to synthesis of toxic compounds. Two of the most pressing issues in microbial interactions are how consortia are established and how we can modulate these microbial communities to express desirable functions. Here, we propose that public goods (i.e., metabolites of high energy demand in biosynthesis) facilitate energy conservation for life under energy-limited conditions and determine the assembly and function of the consortia. Our report suggests that an understanding of public good dynamics could result in new ways to improve microbial pollutant degradation in anaerobic systems.


2020 ◽  
Author(s):  
Michael Baumgartner ◽  
Katia R Pfrunder-Cardozo ◽  
Alex R Hall

AbstractBiological invasions can alter ecosystem stability and function, and predicting what happens when a new species or strain arrives remains a major challenge in ecology. In the mammalian gastrointestinal tract, susceptibility of the resident microbial community to invasion by pathogens has important implications for host health. However, at the community level, it is unclear whether susceptibility to invasion depends mostly on resident community composition (which microbes are present), or also on local abiotic conditions (such as nutrient status). Here, we used a gut microcosm system to disentangle some of the drivers of susceptibility to invasion in microbial communities sampled from humans. We found resident microbial communities inhibited an invading E. coli strain, compared to community-free control treatments, sometimes excluding the invader completely (colonization resistance). These effects were stronger at later time points, coinciding with shifts in microbial community composition and nutrient availability. By separating these two components (microbial community and abiotic environment), we found taxonomic composition played a crucial role in suppressing invasion, but this depended critically on local abiotic conditions (adapted communities were more suppressive in nutrient-depleted conditions). This helps predict when resident communities will be most susceptible to invasion, with implications for optimizing treatments based around microbiota management.


2020 ◽  
Author(s):  
Breah LaSarre ◽  
Adam M. Deutschbauer ◽  
Crystal E. Love ◽  
James B. McKinlay

ABSTRACTMicrobial interactions abound in natural ecosystems and shape community structure and function. Substantial attention has been given to cataloging mechanisms by which microbes interact, but there is a limited understanding of the genetic landscapes that promote or hinder microbial interactions. We previously developed a mutualistic coculture pairing Escherichia coli and Rhodopseudomonas palustris, wherein E. coli provides carbon to R. palustris in the form of glucose fermentation products and R. palustris fixes N2 gas and provides nitrogen to E. coli in the form of NH4+. The stable coexistence and reproducible trends exhibited by this coculture make it ideal for interrogating the genetic underpinnings of a cross-feeding mutualism. Here, we used random barcode transposon sequencing (RB-TnSeq) to conduct a genome-wide search for E. coli genes that influence fitness during cooperative growth with R. palustris. RB-TnSeq revealed hundreds of genes that increased or decreased E. coli fitness in a mutualism-dependent manner. Some identified genes were involved in nitrogen sensing and assimilation, as expected given the coculture design. The other identified genes were involved in diverse cellular processes, including energy production and cell wall and membrane biogenesis. Additionally, we discovered unexpected purine cross-feeding from R. palustris to E. coli, with coculture rescuing growth of an E. coli purine auxotroph. Our data provide insight into the genes and gene networks that can influence a cross-feeding mutualism and underscore that microbial interactions are not necessarily predictable a priori.IMPORTANCEMicrobial communities impact life on earth in profound ways, including driving global nutrient cycles and influencing human health and disease. These community functions depend on the interactions that resident microbes have with the environment and each other. Thus, identifying genes that influence these interactions will aid the management of natural communities and the use of microbial consortia as biotechnology. Here, we identified genes that influenced Escherichia coli fitness during cooperative growth with a mutualistic partner, Rhodospeudomonas palustris. Although this mutualism centers on the bidirectional exchange of essential carbon and nitrogen, E. coli fitness was positively and negatively affected by genes involved in diverse cellular processes. Furthermore, we discovered an unexpected purine cross-feeding interaction. These results contribute knowledge on the genetic foundation of a microbial cross-feeding interaction and highlight that unanticipated interactions can occur even within engineered microbial communities.


2015 ◽  
Author(s):  
Adriana Daudt Grativol ◽  
Albany Marchetti ◽  
Rita M Wetler-Tonini ◽  
Thiago M Venancio ◽  
Carlos EN Gatts ◽  
...  

Mangrove sediment harbors a unique microbiome and is a hospitable environment for the growth of a diverse group of bacteria capable of oil biodegradation. Our goal was to understand bacterial community dynamics from mangrove sediments under heavy-oil contamination stress, and to look for common patterns that may be associated with oil biodegradation is such environments. We tested the hypothesis of a two-phase pattern of petroleum biodegradation, already reported in the literature, where key events in the degradation process take place in the first three weeks after the contamination. Two sample sites with different oil pollution history were compared through T-RFLP analyses and using a pragmatic approach based on the Microbial Resource Management Framework. Our data corroborated the already reported two-phase pattern of oil biodegradation, although the original proposed explanation is questioned, opening up the possibility to consider other plausible hypothesis of microbial interactions as the main drivers of this pattern.


PeerJ ◽  
2018 ◽  
Vol 6 ◽  
pp. e4975 ◽  
Author(s):  
Bo Zhang ◽  
Lijuan Yan ◽  
Qiang Li ◽  
Jie Zou ◽  
Hao Tan ◽  
...  

BackgroundGanoderma lucidum, a valuable medicinal fungus, is widely distributed in China. It grows alongside with a complex microbial ecosystem in the substrate. As sequencing technology advances, it is possible to reveal the composition and functions of substrate-associated bacterial communities.MethodsWe analyzed the bacterial community dynamics in the substrate during the four typical growth stages ofG. lucidumusing next-generation sequencing.ResultsThe physicochemical properties of the substrate (e.g. acidity, moisture, total nitrogen, total phosphorus and total potassium) changed between different growth stages. A total of 598,771 sequences from 12 samples were obtained and assigned to 22 bacterial phyla.ProteobacteriaandFirmicuteswere the dominant phyla. Bacterial community composition and diversity significantly differed between the elongation stage and the other three growth stages. LEfSe analysis revealed a large number of bacterial taxa (e.g.Bacteroidetes,AcidobacteriaandNitrospirae) with significantly higher abundance at the elongation stage. Functional pathway prediction uncovered significant abundance changes of a number of bacterial functional pathways between the elongation stage and other growth stages. At the elongation stage, the abundance of the environmental information processing pathway (mainly membrane transport) decreased, whereas that of the metabolism-related pathways increased.DiscussionThe changes in bacterial community composition, diversity and predicted functions were most likely related to the changes in the moisture and nutrient conditions in the substrate with the growth ofG. lucidum, particularly at the elongation stage. Our findings shed light on theG. lucidum-bacteria-substrate relationships, which should facilitate the industrial cultivation ofG. lucidum.


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