Bacterial co-culture with cell signaling translator and growth controller modules for autonomously regulated culture composition

Stephens, Kristina; Pozo, Maria; Tsao, Chen‐Yu; Hauk, Pricila; Bentley, William E.

doi:10.1038/s41467-019-12027-6

Cited by 100 publications

(92 citation statements)

References 47 publications

(53 reference statements)

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“…Surprisingly, the role and the consequence of the QS molecules, well described in pure culture, are poorly investigated and understood in bacterial consortia, closer to those found in Nature. Recently one study investigates this question using mathematical model to demonstrate/ propose how QS control the population trajectories in synthetic consortium 33 .…”

Section: Discussionmentioning

confidence: 99%

Metabolic exchange and energetic coupling between nutritionally stressed bacterial species, the possible role of QS molecules

Ranava

Backes

Karthikeyan

et al. 2020

Preprint

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To clarify the principles controlling inter-species interactions, we previously developed a co-culture model with two anaerobic bacteria, Clostridium acetobutylicum and Desulfovibrio vulgaris Hildenborough, in which nutritional stress for D. vulgaris induced tight cell-cell inter-species interaction. Here we show that exchange of metabolites produced by C. acetobutylicum allows D. vulgaris to duplicate its DNA, and to be energetically viable even without its substrates. Physical interaction between C. acetobutylicum and D. vulgaris (or Escherichia coli and D. vulgaris) is linked to the quorum-sensing molecule AI-2, produced by C. acetobutylicum and E. coli. With nutrients D. vulgaris produces a small molecule that inhibits in vitro the AI-2 activity, and could act as an antagonist in vivo. Sensing of AI-2 by D.vulgaris could induce formation of an intercellular structure that allows directly or indirectly metabolic exchange and energetic coupling between the two bacteria.To further investigate interactions between bacterial species we developed a synthetic microbial consortium constituted by two species: C. acetobutylicum, Gram-positive, and D. vulgaris, Gram-negative, sulfate reducing. There are both involved in anaerobic digestion of organic waste matter 16,17 . Glucose, a substrate that cannot be used by D. vulgaris 16 , is the sole carbon source in the consortium, and the consortium produces three times more H 2 than C. acetobutylicum alone, D. vulgaris even grows in the absence of sulphate, its final electron acceptor for the respiration process 18 . Although D. vulgaris can ferment lactate, a metabolite produced by C. acetobutylicum, this process is greatly inhibited by high H 2 concentrations, preventing D. vulgaris from growing in the absence of methanogens 19 . We observed a form of bacterial communication between adjacent cells of both types of bacteria by cell-cell interaction, in conditions of nutritional stress, with exchange in both directions of cell material, associated with the modification of the metabolism evidenced by a higher production of CO 2 and H 2 18 . In some cases, the interactions between C. acetobutylicum and D. vulgaris, resembled those described by Dubey and Ben-Yehuda 10 . Moreover, this type of cellcell interactions has been seen also in other systems, which give support to its existence and functionality 10,13 .Nutritional stress appears crucial to induce physical contact between bacteria, as this interaction was prevented by the presence of lactate and sulfate, nutrients of D. vulgaris.Furthermore, Pande et al 20 in a synthetic co-culture of E. coli and Acinetobacter baylyi, after depletion of aminoacids such as histidine and tryptophan by genetic manipulation, observed nanotubular structures between the auxotrophs allowing cytoplasmic exchange. As in our case, the communication between the mutants was prevented by the presence of the nutrients.The formation of nanotubes between aminoacid-starved bacteria might be a strategy to survive under aminoacid limiting conditions 13 . F...

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Section: Discussionmentioning

confidence: 99%

Metabolic exchange and energetic coupling between nutritionally stressed bacterial species, the possible role of QS molecules

Ranava

Backes

Karthikeyan

et al. 2020

Preprint

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“…The expression of a burdensome heterologous circuit was regulated, switching between "growth mode" and "production mode" in response to population density (Gupta et al, 2017). It has also been demonstrated that control over the growth rates of one strain, through modulating expression of the ptsH sugar transport gene, can be used to control the composition of co-cultures (Stephens et al, 2019). A similar approach was used to distribute a naringenin production pathway between two strains (Dinh et al, 2020).…”

Section: Building Stable Communitiesmentioning

confidence: 99%

From Microbial Communities to Distributed Computing Systems

Karkaria¹,

Treloar²,

Barnes³

et al. 2020

Front. Bioeng. Biotechnol.

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A distributed biological system can be defined as a system whose components are located in different subpopulations, which communicate and coordinate their actions through interpopulation messages and interactions. We see that distributed systems are pervasive in nature, performing computation across all scales, from microbial communities to a flock of birds. We often observe that information processing within communities exhibits a complexity far greater than any single organism. Synthetic biology is an area of research which aims to design and build synthetic biological machines from biological parts to perform a defined function, in a manner similar to the engineering disciplines. However, the field has reached a bottleneck in the complexity of the genetic networks that we can implement using monocultures, facing constraints from metabolic burden and genetic interference. This makes building distributed biological systems an attractive prospect for synthetic biology that would alleviate these constraints and allow us to expand the applications of our systems into areas including complex biosensing and diagnostic tools, bioprocess control and the monitoring of industrial processes. In this review we will discuss the fundamental limitations we face when engineering functionality with a monoculture, and the key areas where distributed systems can provide an advantage. We cite evidence from natural systems that support arguments in favor of distributed systems to overcome the limitations of monocultures. Following this we conduct a comprehensive overview of the synthetic communities that have been built to date, and the components that have been used. The potential computational capabilities of communities are discussed, along with some of the applications that these will be useful for. We discuss some of the challenges with building co-cultures, including the problem of competitive exclusion and maintenance of desired community composition. Finally, we assess computational frameworks currently available to aide in the design of microbial communities and identify areas where we lack the necessary tools.

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“…Centralized treatment plants can then monitor and mediate chemical run-off using networked biological-pods, (“bPods”), equipped with electrochemical sensors, engineered cells, and wireless transmitters ( Stine et al., 2020 ). Similar devices, or in-line microfluidic devices ( Shang et al., 2019 ), could also be used to electronically monitor molecular communication in biomanufacturing with the potential to monitor multiple media components simultaneously, and to direct metabolic use of engineered strains ( Stephens et al., 2019 ; Tsao et al., 2010 ). Each of these systems demonstrates that either in single devices, or networked devices, there are immediate applications for electronically actuated biomolecular communication.…”

Section: Introductionmentioning

confidence: 99%

Redox Electrochemistry to Interrogate and Control Biomolecular Communication

et al. 2020

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Summary Cells often communicate by the secretion, transport, and perception of molecules. Information conveyed by molecules is encoded, transmitted, and decoded by cells within the context of the prevailing microenvironments. Conversely, in electronics, transmission reliability and message validation are predictable, robust, and less context dependent. In turn, many transformative advances have resulted by the formal consideration of information transfer. One way to explore this potential for biological systems is to create bio-device interfaces that facilitate bidirectional information transfer between biology and electronics. Redox reactions enable this linkage because reduction and oxidation mediate communication within biology and can be coupled with electronics. By manipulating redox reactions, one is able to combine the programmable features of electronics with the ability to interrogate and modulate biological function. In this review, we examine methods to electrochemically interrogate the various components of molecular communication using redox chemistry and to electronically control cell communication using redox electrogenetics.

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Bacterial co-culture with cell signaling translator and growth controller modules for autonomously regulated culture composition

Cited by 100 publications

References 47 publications

Metabolic exchange and energetic coupling between nutritionally stressed bacterial species, the possible role of QS molecules

Metabolic exchange and energetic coupling between nutritionally stressed bacterial species, the possible role of QS molecules

From Microbial Communities to Distributed Computing Systems

Redox Electrochemistry to Interrogate and Control Biomolecular Communication

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