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

Fazzino, Lisa; Anisman, Jeremy; Chacón, Jeremy M.; Heineman, Richard H.; Harcombe, William R.

doi:10.1038/s41396-019-0511-z

Cited by 47 publications

(33 citation statements)

References 44 publications

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“…The turnover of biomass from the primary resource population and the release of necromass is a common mechanism in natural consortia and can drive flux of material and energy between trophic levels [64][65][66][67][68] . Biomass turnover, through mechanisms like senescence, inhibitor-based cell lysis, or viral predation, can result in increased energy acquisition rates in the systems.…”

Section: Discussionmentioning

confidence: 99%

Artificial consortium demonstrates emergent properties of enhanced cellulosic-sugar degradation and biofuel synthesis

Park

Patel

Hunt

et al. 2020

npj Biofilms Microbiomes

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Planktonic cultures, of a rationally designed consortium, demonstrated emergent properties that exceeded the sums of monoculture properties, including a >200% increase in cellobiose catabolism, a >100% increase in glycerol catabolism, a >800% increase in ethanol production, and a >120% increase in biomass productivity. The consortium was designed to have a primary and secondary-resource specialist that used crossfeeding with a positive feedback mechanism, division of labor, and nutrient and energy transfer via necromass catabolism. The primary resource specialist was Clostridium phytofermentans (a.k.a. Lachnoclostridium phytofermentans), a cellulolytic, obligate anaerobe. The secondary-resource specialist was Escherichia coli, a versatile, facultative anaerobe, which can ferment glycerol and byproducts of cellobiose catabolism. The consortium also demonstrated emergent properties of enhanced biomass accumulation when grown as biofilms, which created high cell density communities with gradients of species along the vertical axis. Consortium biofilms were robust to oxic perturbations with E. coli consuming O2, creating an anoxic environment for C. phytofermentans. Anoxic/oxic cycling further enhanced biomass productivity of the biofilm consortium, increasing biomass accumulation ~250% over the sum of the monoculture biofilms. Consortium emergent properties were credited to several synergistic mechanisms. E. coli consumed inhibitory byproducts from cellobiose catabolism, driving higher C. phytofermentans growth and higher cellulolytic enzyme production, which in turn provided more substrate for E. coli. E. coli necromass enhanced C. phytofermentans growth while C. phytofermentans necromass aided E. coli growth via the release of peptides and amino acids, respectively. In aggregate, temporal cycling of necromass constituents increased flux of cellulose-derived resources through the consortium. The study establishes a consortia-based, bioprocessing strategy built on naturally occurring interactions for improved conversion of cellulose-derived sugars into bioproducts.

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Section: Discussionmentioning

confidence: 99%

Artificial consortium demonstrates emergent properties of enhanced cellulosic-sugar degradation and biofuel synthesis

Park

Patel

Hunt

et al. 2020

npj Biofilms Microbiomes

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“…Any well that had an OD 600 or fluorescent protein value above 10% of the highest plate value was considered growth. We used the highest plate value rather than the antibiotic-free well because we consistently saw a slight increase in OD 600 in the cocultures at sublethal concentrations, possibly due to a low level of cell lysis and a subsequent boost for the cross-feeding partner ( 61 , 62 ).…”

Section: Methodsmentioning

confidence: 99%

Weakest-Link Dynamics Predict Apparent Antibiotic Interactions in a Model Cross-Feeding Community

Adamowicz

Harcombe

2020

Antimicrob Agents Chemother

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With the growing global threat of antimicrobial resistance, novel strategies are required for combatting resistant pathogens. Combination therapy, wherein multiple drugs are used to treat an infection, has proven highly successful in the treatment of cancer and HIV. However, this practice has proven challenging for the treatment of bacterial infections due to difficulties in selecting the correct combinations and dosages. An additional challenge in infection treatment is the polymicrobial nature of many infections, which may respond to antibiotics differently than a monoculture pathogen. This study tests whether patterns of antibiotic interactions (synergy, antagonism, or independence/additivity) in monoculture can be used to predict antibiotic interactions in an obligate cross-feeding co-culture. Using our previously described weakest link hypothesis, we hypothesized antibiotic interactions in co-culture based on the interactions we observed in monoculture. We then compared our predictions to observed antibiotic interactions in co-culture. We tested the interactions between ten previously identified antibiotic combinations using checkerboard assays. Although our antibiotic combinations interacted differently than predicted in our monocultures, our monoculture results were generally sufficient to predict co-culture patterns based solely on the weakest link hypothesis. These results suggest that combination therapy for cross-feeding multispecies infections may be successfully designed based on antibiotic interaction patterns for their component species.

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“…Sequence analysis was performed using BreSeq [61] to align Illumina reads to reference E. coli and S. enterica genomes as previously described [62]. Briefly, mutation lists for resistant populations were filtered such that variation between our ancestral strains and the reference genome were removed, as well as any mutations which also arose in the antibiotic-free populations.…”

Section: Sequencingmentioning

confidence: 99%

Cross-feeding modulates the rate and mechanism of antibiotic resistance evolution in a model microbial community of Escherichia coli and Salmonella enterica

et al. 2020

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With antibiotic resistance rates on the rise, it is critical to understand how microbial species interactions influence the evolution of resistance. In obligate mutualisms, the survival of any one species (regardless of its intrinsic resistance) is contingent on the resistance of its cross-feeding partners. This sets the community antibiotic sensitivity at that of the 'weakest link' species. In this study, we tested the hypothesis that weakest link dynamics in an obligate cross-feeding relationship would limit the extent and mechanisms of antibiotic resistance evolution. We experimentally evolved an obligate co-culture and monoculture controls along gradients of two different antibiotics. We measured the rate at which each treatment increased antibiotic resistance, and sequenced terminal populations to question whether mutations differed between mono-and co-cultures. In both rifampicin and ampicillin treatments, we observed that resistance evolved more slowly in obligate co-cultures of E. coli and S. enterica than in monocultures. While we observed similar mechanisms of resistance arising under rifampicin selection, under ampicillin selection different resistance mechanisms arose in co-cultures and monocultures. In particular, mutations in an essential cell division protein, ftsI, arose in S. enterica only in co-culture. A simple mathematical model demonstrated that reliance on a partner is sufficient to slow the rate of adaptation, and can change the distribution of adaptive mutations that are acquired. Our results demonstrate that cooperative metabolic interactions can be an important modulator of resistance evolution in microbial communities.

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

Cited by 47 publications

References 44 publications

Artificial consortium demonstrates emergent properties of enhanced cellulosic-sugar degradation and biofuel synthesis

Artificial consortium demonstrates emergent properties of enhanced cellulosic-sugar degradation and biofuel synthesis

Weakest-Link Dynamics Predict Apparent Antibiotic Interactions in a Model Cross-Feeding Community

Cross-feeding modulates the rate and mechanism of antibiotic resistance evolution in a model microbial community of Escherichia coli and Salmonella enterica

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