Engineered Interspecies Amino Acid Cross-Feeding Increases Population Evenness in a Synthetic Bacterial Consortium

Ziesack, Marika; Gibson, Travis E.; Oliver, John K.W.; Shumaker, Andrew M.; Hsu, Bryan B.; Riglar, David T.; Giessen, Tobias W.; DiBenedetto, Nicholas; Bry, Lynn; Way, Jeffrey C.; Silver, Pamela A.; Gerber, Georg K.

doi:10.1128/msystems.00352-19

Cited by 49 publications

(40 citation statements)

References 47 publications

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“…Moreover, the cross-feeding of this eAA, most likely, occurs also in vivo, since Lp levels are higher in biassociated than in monoassociated flies deprived of Ile, and Lp is necessary with Ap for altering feeding behaviour and egg laying in these flies. Microbial cross-feeding has been shown to allow intra-and inter-species exchange of several nutrients, including AAs, through its secretion to the media or via bacterial nanotubes 65,73,74 . The Ap-Lp interaction is however not unidirectional as has been shown for example for yeast-Lactobacilli interactions 75 .…”

Section: Discussionmentioning

confidence: 99%

Metabolic cross-feeding in imbalanced diets allows gut microbes to improve reproduction and alter host behaviour

et al. 2020

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The impact of commensal bacteria on the host arises from complex microbial-diet-host interactions. Mapping metabolic interactions in gut microbial communities is therefore key to understand how the microbiome influences the host. Here we use an interdisciplinary approach including isotope-resolved metabolomics to show that in Drosophila melanogaster, Acetobacter pomorum (Ap) and Lactobacillus plantarum (Lp) a syntrophic relationship is established to overcome detrimental host diets and identify Ap as the bacterium altering the host's feeding decisions. Specifically, we show that Ap uses the lactate produced by Lp to supply amino acids that are essential to Lp, allowing it to grow in imbalanced diets. Lactate is also necessary and sufficient for Ap to alter the fly's protein appetite. Our data show that gut bacterial communities use metabolic interactions to become resilient to detrimental host diets. These interactions also ensure the constant flow of metabolites used by the microbiome to alter reproduction and host behaviour.

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Section: Discussionmentioning

confidence: 99%

Metabolic cross-feeding in imbalanced diets allows gut microbes to improve reproduction and alter host behaviour

et al. 2020

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“…Among the hits from our screen, we were most intrigued by the genes exhibiting mutualism-abolished fitness defects ( Table 2 ) because, unlike some other coculture systems (18, 46, 65), our coculture does not enforce coexistence through an engineered auxotrophy. One mechanism by which coculturing could restore E. coli mutant fitness is by slowing the growth of all E. coli strains.…”

Section: Resultsmentioning

confidence: 99%

Genome-wide analysis ofEscherichia colifitness determinants in a cross-feeding mutualism withRhodopseudomonas palustris

LaSarre

Deutschbauer

Love

et al. 2020

Preprint

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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. 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.

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“…33 ) that multicellular systems operating for several days exhibited reasonable stability. If needed, synthetic cooperative behavior could be used to maintain all strains in the population 54,55 . Strains could also be cultivated in separate chambers within a microfluidic device for instance, avoiding competition problems 56 .…”

Section: Discussionmentioning

confidence: 99%

Rational programming of history-dependent logic in cellular populations

et al. 2020

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Genetic programs operating in a history-dependent fashion are ubiquitous in nature and govern sophisticated processes such as development and differentiation. The ability to systematically and predictably encode such programs would advance the engineering of synthetic organisms and ecosystems with rich signal processing abilities. Here we implement robust, scalable history-dependent programs by distributing the computational labor across a cellular population. Our design is based on standardized recombinase-driven DNA scaffolds expressing different genes according to the order of occurrence of inputs. These multicellular computing systems are highly modular, do not require cell-cell communication channels, and any program can be built by differential composition of strains containing well-characterized logic scaffolds. We developed automated workflows that researchers can use to streamline program design and optimization. We anticipate that the history-dependent programs presented here will support many applications using cellular populations for material engineering, biomanufacturing and healthcare.

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Engineered Interspecies Amino Acid Cross-Feeding Increases Population Evenness in a Synthetic Bacterial Consortium

Cited by 49 publications

References 47 publications

Metabolic cross-feeding in imbalanced diets allows gut microbes to improve reproduction and alter host behaviour

Metabolic cross-feeding in imbalanced diets allows gut microbes to improve reproduction and alter host behaviour

Genome-wide analysis ofEscherichia colifitness determinants in a cross-feeding mutualism withRhodopseudomonas palustris

Rational programming of history-dependent logic in cellular populations

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