Microbial domestication signatures of <i>Lactococcus lactis</i> can be reproduced by experimental evolution

Bachmann, Herwig; Starrenburg, Marjo; Molenaar, Douwe; Kleerebezem, Michiel; Vlieg, Johan E. T. van Hylckama

doi:10.1101/gr.121285.111

Cited by 153 publications

(142 citation statements)

References 57 publications

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“…Because of this burden the expression of extracellular proteases in lactococci (31,32), invertase expression in yeast (33), or siderophore production in the pathogen Pseudomonas aeruginosa (34) are described as unstable. Such cooperative traits are expected to behave fundamentally differently in a suspension compared with an emulsion-based culturing system.…”

Section: Discussionmentioning

confidence: 99%

Availability of public goods shapes the evolution of competing metabolic strategies

Bachmann¹,

Fischlechner

Rabbers³

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Tradeoffs provide a rationale for the outcome of natural selection. A prominent example is the negative correlation between the growth rate and the biomass yield in unicellular organisms. This tradeoff leads to a dilemma, where the optimization of growth rate is advantageous for an individual, whereas the optimization of the biomass yield would be advantageous for a population. High-rate strategies are observed in a broad variety of organisms such as Escherichia coli, yeast, and cancer cells. Growth in suspension cultures favors fast-growing organisms, whereas spatial structure is of importance for the evolution of high-yield strategies. Despite this realization, experimental methods to directly select for increased yield are lacking. We here show that the serial propagation of a microbial population in a water-in-oil emulsion allows selection of strains with increased biomass yield. The propagation in emulsion creates a spatially structured environment where the growth-limiting substrate is privatized for populations founded by individual cells. Experimental evolution of several isogenic Lactococcus lactis strains demonstrated the existence of a tradeoff between growth rate and biomass yield as an apparent Pareto front. The underlying mutations altered glucose transport and led to major shifts between homofermentative and heterofermentative metabolism, accounting for the changes in metabolic efficiency. The results demonstrated the impact of privatizing a public good on the evolutionary outcome between competing metabolic strategies. The presented approach allows the investigation of fundamental questions in biology such as the evolution of cooperation, cell-cell interactions, and the relationships between environmental and metabolic constraints.A lthough the existence of tradeoffs in evolution seems to be undisputable, experimental evidence obtained under controlled conditions is scarce. Several examples failed to show tradeoffs (1-4), whereas others could find them (5, 6) or found general but not universal tradeoffs (7,8). A tradeoff between growth rate and growth yield in microbes (9-11) has direct implications for experiments carried out in liquid cultures. This is especially of importance during prolonged cultivations such as laboratory evolution experiments. In suspension, fast-growing variants outcompete slower growing ones at the cost of biomass yield (5). The yield versus rate optimization is governed by a dilemma where fast growth is advantageous from the perspective of an individual cell, whereas slow growth, and therefore high yield, is advantageous from the perspective of a population. This dilemma is consistent with a concept termed the tragedy of the commons (12). It is well described that spatial structure is essential for the selection of high-yield strategies (13-15). The yield/rate tradeoff of microbial growth has been linked to metabolic strategies (11) such as the switch between respiration and fermentation in yeast (9). It is suggested that the underlying cause of this tradeoff is based on...

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Section: Discussionmentioning

confidence: 99%

Availability of public goods shapes the evolution of competing metabolic strategies

Bachmann¹,

Fischlechner

Rabbers³

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

176

220

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“…Lactococcus lactis is a LAB species growing in a variety of niches. It is frequently encountered on vegetable substrates as well as in the dairy environment (Bachmann et al, 2012;Kelly et al, 2010).…”

Section: Dynamics Of Microbial Community During the Whole Fermentationmentioning

confidence: 99%

Characterization of Microbial Community during the Fermentation of Chinese Homemade <i>paocai</i>, a Traditional Fermented Vegetable Food

Liang¹,

Zhang²,

Wu³

et al. 2016

FSTR

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“…The plasmid-borne nature of the lactose metabolism and/or proteinase determinants on large plasmids in certain Lactococcus strains is well established (Gasson, 1983;Maeda & Gasson, 1986;McKay et al, 1976). These large plasmids are subject to spontaneous loss or frequent deletions (Bachmann et al, 2012;McKay & Baldwin, 1974), with obvious consequences for the industrial processes that they are involved in. All these genetic events involving plasmids led to a wide diversity of phenotypes among lactococci strains.…”

Section: Introductionmentioning

confidence: 99%

Molecular characterization and structural instability of the industrially important composite metabolic plasmid pLP712

et al. 2012

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The widely used plasmid-free Lactococcus lactis strain MG1363 was derived from the industrial dairy starter strain NCDO712. This strain carries a 55.39 kb plasmid encoding genes for lactose catabolism and a serine proteinase involved in casein degradation. We report the DNA sequencing and annotation of pLP712, which revealed additional metabolic genes, including peptidase F, D-lactate dehydrogenase and a-keto acid dehydrogenase (E3 complex). Comparison of pLP712 with other large lactococcal lactose and/or proteinase plasmids from L. lactis subsp. cremoris SK11 (pSK11L, pSK11P) and the plant strain L. lactis NCDO1867 (pGdh442) revealed their close relationship. The plasmid appears to have evolved through a series of genetic events as a composite of pGdh442, pSK11L and pSK11P. We describe in detail a scenario by which the metabolic genes relevant to the growth of its host in a milk environment have been unified on one replicon, reflecting the evolution of L. lactis as it changed its biological niche from plants to dairy environments. The extensive structural instability of pLP712 allows easy isolation of derivative plasmids lacking genes for casein degradation and/or lactose catabolism. Plasmid pLP712 is transferable by transduction and conjugation, and both of these processes result in significant molecular rearrangements. We report the detailed molecular analysis of insertion sequence element-mediated genetic rearrangements within pLP712 and several different mechanisms, including homologous recombination and adjacent deletion. Analysis of the integration of the lactose operon into the chromosome highlights the fluidity of the MG1363 integration hotspot and the potential for frequent movement of genes between plasmids and chromosomes in Lactococcus.

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Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution

Cited by 153 publications

References 57 publications

Availability of public goods shapes the evolution of competing metabolic strategies

Availability of public goods shapes the evolution of competing metabolic strategies

Characterization of Microbial Community during the Fermentation of Chinese Homemade <i>paocai</i>, a Traditional Fermented Vegetable Food

Molecular characterization and structural instability of the industrially important composite metabolic plasmid pLP712

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