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Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution
Open accessAbstract
Experimental evolution is a powerful approach to unravel how selective forces shape microbial genotypes and phenotypes. To this date, the available examples focus on the adaptation to conditions specific to the laboratory. The lactic acid bacterium Lactococcus lactis naturally occurs on plants and in dairy environments, and it is proposed that dairy strains originate from the plant niche. Here we investigate the adaptation of a L. lactis strain isolated from a plant to a dairy niche by propagating it for 1000 generations in milk. Two out of three independently evolved strains displayed significantly increased acidification rates and biomass yields in milk. Genome resequencing, revealed six, seven, and 28 mutations in the three strains, including point mutations in loci related to amino acid biosynthesis and transport and in the gene encoding MutL, which is involved in DNA mismatch repair. Two strains lost a conjugative transposon containing genes important in the plant niche but dispensable in milk. A plasmid carrying an extracellular protease was introduced by transformation. Although improving growth rate and growth yield significantly, the plasmid was rapidly lost. Comparative transcriptome and phenotypic analyses confirmed that major physiological changes associated with improved growth in milk relate to nitrogen metabolism and the loss or down-regulation of several pathways involved in the utilization of complex plant polymers. Reproducing the transition from the plant to the dairy niche through experimental evolution revealed several genome, transcriptome, and phenotype signatures that resemble those seen in strains isolated from either niche.
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TL;DR
Propagating the plant isolate *Lactococcus lactis* KF147 in milk for 1000 generations reproduced several genomic, transcriptomic, and phenotypic signatures of dairy domestication, including improved growth and mutations in nitrogen metabolism. Two of three independently evolved strains grew significantly better in milk, and one became a mutator via a *mutL* deletion.
Key findings
- After 1000 generations, two of three adapted strains had significantly increased acidification and biomass yield in milk: maximum cell density was 2.0-fold higher for NZ5521 (p = 0.006), 2.8-fold for NZ5522 (p < 0.001), and 1.41-fold for NZ5523 (p = 0.31) versus KF147; relative fitness was 1.48, 1.1, and 1.21, respectively.
- Genome resequencing found 21, 4, and 6 SNPs in NZ5521, NZ5522, and NZ5523, plus 7 and 2 INDELs in NZ5521 and NZ5522; NZ5522 and NZ5523 lost an identical 51.3-kb Tn6098-like conjugative transposon. NZ5521 had a *mutL* deletion and a ~10-fold higher mutation frequency (10.02 vs. 1.34 × 10⁻⁷ mutations/generation for KF147).
- The protease plasmid pNZ521 improved growth but was rapidly lost; no protease-positive strains were detected after 1000 generations. Transcriptome analysis found 291 of 1850 genes differentially expressed (p < 0.001), with an oligopeptide ABC transporter operon upregulated in NZ5521/NZ5522 via identical *oppD*/*oppC* upstream deletions, and plant-polymer utilization pathways downregulated, converging toward dairy strain IL594.
Methods
- Experimental evolution: *L. lactis* KF147, a mung-bean sprout isolate carrying pNZ521, was serially propagated in reconstituted skimmed milk in three parallel cultures (SP1–SP3) for 1000 generations (~16.6 generations per transfer; effective population size 1.66 × 10⁶). After 300 generations, protease-positive cells were selected and further propagated.
- Phenotypic and genomic characterization: acidification, CFU, and competition fitness assays; Illumina whole-genome resequencing with PCR/amplicon validation; fluctuation analysis for mutation rates.
- Transcriptome analysis: custom Agilent microarrays comparing adapted strains, KF147, KF147_PRT, and dairy isolate IL594 during exponential growth in milk, using 1850 genes covered by 100% matching probes.
Limitations
- Stated: the 300-generation bottleneck (only ~100 protease-positive colonies per culture) may have lost beneficial mutations; *oppC* probe mismatch may underestimate IL594 expression; averaged P-values are not FDR-corrected; the authors cannot exclude that the GadR homolog regulates additional genes.
- Evident: the study uses one plant isolate, three evolved lines, and one clone per line under laboratory milk conditions, so it does not directly demonstrate the natural plant-to-dairy transition.
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In the paper
“It should be noted that the competition experiments using the strains KF147, NZ5521, NZ5522, and NZ5523 in coculture with the protease-positive dairy isolate IL594 (Chopin et al. 1984) did not reveal a fitness difference for any of the tested combinations (data not shown).”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Increased growth rate, yield, and fitness of mutants in milk
What the sources say
- Not checked yetcites Chopin et al. 1984
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In the paper
“Since Tn6098 contains the only predicted a-galactosidase of the parental KF147 strain”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Adaptation resulted in the loss of mobile elements and generation of a mutator strain
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“Notably, the introduction of a plasmid, pNZ521 (de Vos et al. 1989), encoding the lactococcal extracellular protease (PrtP) in strain KF147 significantly enhanced growth in milk (Fig. 1A).”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Results
What the sources say
- Not checked yetcites de Vos et al. 1989
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“As expected for a strain with defects in DNA mismatch repair, the majority of mutations (15 out of 21) in strain NZ5521 were A:T 4 G:C transitions (Miller 1996).”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Experimental evolution of dairy lactococci
What the sources say
- Not checked yetcites Miller 1996
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In the paper
“Additionally, identical single-base deletions were identified in strains NZ5521 and NZ5522 upstream of the fourth gene in this operon (oppC).”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Transcriptome of two adapted strains converges toward that of a dairy strain
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In the paper
“It grows poorly in milk as compared to typical dairy L. lactis strains.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Results
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In the paper
“It was also expressed at a significantly increased level in strains NZ5521 and NZ5522 (Fig. 2, cluster 7).”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Transcriptome of two adapted strains converges toward that of a dairy strain
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In the paper
“In the ancestral strain KF147, oppC is annotated as a pseudogene, which due to a frameshift encodes an N-terminally truncated version of the conserved OppC protein, the permease subunit of the oligopeptide ABC transporter.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Transcriptome of two adapted strains converges toward that of a dairy strain
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In the paper
“The transcription level of a locus encoding genes involved in Branched Chain Amino Acid (BCAA) (leucine, valine, isoleucine) biosynthesis was significantly increased in strains NZ5521 and NZ5523.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Transcriptome of two adapted strains converges toward that of a dairy strain
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In the paper
“In contrast, the same locus was transcribed at slightly lower levels in strains NZ5522 and in KF147_PRT (Supplemental Fig. 6).”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Transcriptome of two adapted strains converges toward that of a dairy strain
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- It may state two separate claims as one. 30
- Probably not a substantial claim. 19
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The relative fitness was 1.48 ( p > 0.000), 1.1 ( p = 0.037), and 1.21 ( p = 0.009) for strains NZ5521, NZ5522, and NZ5523, respectively (Supplemental Fig. 2).”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Increased growth rate, yield, and fitness of mutants in milk
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In the paper
“Additionally, a transcriptional regulator of the RpiR family, which has been described to regulate phospho-sugar metabolism in E. coli (Sorensen and Hove-Jensen 1996), as well as a transcriptional regulator involved in fructose/lactose transport were down-regulated in the adapted strains and in IL594.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Experimental evolution of dairy lactococci
What the sources say
- Not checked yetcites Sorensen and Hove-Jensen 1996
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In the paper
“NZ5523 shares loss of Tn6098 with NZ5522, but none of the other mutations occurred in both strains.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Experimental evolution of dairy lactococci
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In the paper
“Furthermore, genes involved in the utilization of plant polymers like a-and b-glucosides as well as genes involved in uronic acid metabolism display decreased transcription levels in NZ5521, NZ5522, and IL594, which is in agreement with their redundancy in a dairy environment.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Experimental evolution of dairy lactococci
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In the paper
“Notably, the strains NZ5521 and NZ5522 reached their maximum cell density within 24 h of cultivation, while with NZ5523 and the parental KF147, this took more than 2 d (Supplemental Fig. 1).”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Increased growth rate, yield, and fitness of mutants in milk
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In the paper
“The acidification rates of NZ5521 and NZ5522 were increased as compared with KF147, whereas the acidification rate of NZ5523 was only slightly increased (Fig. 1C).”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Increased growth rate, yield, and fitness of mutants in milk
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In the paper
“Acidification rates were rapid during the initial cultivations, whereas they decreased after 300 generations (Fig. 1A).”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Results
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In the paper
“Two point mutations were identified in the NZ5521 genome within the promoter region of a putative transcriptional repressor of the Rgg/GadR/MutR family, one of which was also found in strain NZ5522.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Experimental evolution of dairy lactococci
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In the paper
“Further propagation of proteasepositive cells revealed that the proteolytic trait could not be stabilized in any of these cultures, and that it was lost at a similar rate as observed during the first 300 generations.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Results
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In the paper
“In addition to truncation of a phosphonate ABC transporter, the other two genes affected in NZ5523 are an oligopeptide transporter and a transcriptional regulator of the DeoR family, which is described to regulate sugar catabolism.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Experimental evolution of dairy lactococci
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In the paper
“Compared with KF147, the maximum cell density reached by the adapted strains was 2.0-fold ( p = 0.006), 2.8-fold ( p < 0.001), and 1.41-fold ( p = 0.31) higher for NZ5521, NZ5522, and NZ5523, respectively.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Increased growth rate, yield, and fitness of mutants in milk
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In the paper
“| NZ5521 24 | 10.02 | 9.30 | 10.76 |”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Array data analysis
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In the paper
“This strategy allowed the confirmation of all except one incorrectly predicted INDEL mutation.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Genotypic characterization
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In the paper
“| NZ5522 24 | 1.14 | 0.96 | 1.32 |”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Array data analysis
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In the paper
“Many of the putative genes not represented on the array were relatively short: 55% had less than 50 amino acids, and 80% had less than 100 amino acids, indicating that not all of them might be coding genes.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Design of microarrays
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In the paper
“| NZ5523 24 | 1.06 | 0.90 | 1.22 |”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Array data analysis
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In the paper
“This gene shares 41% protein sequence identity with GadR in L. lactis MG1363, which has been shown to regulate the expression of the gadCB operon, involved in glutamate-dependent acid resistance (Sanders et al. 1998).”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Experimental evolution of dairy lactococci
What the sources say
- Not checked yetcites Sanders et al. 1998
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In the paper
“Therefore, despite the smaller phenotypic changes detected in NZ5523, the mutations identified in this adapted strain are also related to nitrogen and carbohydrate metabolism, which is consistent with multiple mutations selected in strains NZ5521 and NZ5522.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Experimental evolution of dairy lactococci
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In the paper
“L. lactis KF147 was isolated from mung-bean sprouts (Kelly et al. 1998;Siezen et al. 2008).”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Results
What the sources say
- Not checked yetcites Kelly et al. 1998
- Not checked yetcites Siezen et al. 2008
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In the paper
“The single base-pair deletion identified in NZ5521 and NZ5522 restores the normal full-length oppC gene and thereby probably restores its functionality (Fig. 3; Supplemental Fig. 5).”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Transcriptome of two adapted strains converges toward that of a dairy strain
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In the paper
“The reduced expression of sugar transport systems like the cellobiose-PTS may result from the absence of cellobiose in milk, while this disaccharide can be found in plant-derived materials as a degradation product of cellulose.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Transcriptome of two adapted strains converges toward that of a dairy strain
Strength:hedged· not yet calibratedCausal:conditional· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✗ Based: failsProbably not a substantial claim. The paper’s conclusions may not depend on it. The paper may give no reason why it holds. It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“This mutation leads to a 200-amino-acid truncation of the encoded protein that most likely renders it non-functional, potentially explaining the increased mutation rate.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Experimental evolution of dairy lactococci
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In the paper
“The almost simultaneous loss of transposon Tn6098 in cultures SP2 and SP3 indicates that the genes associated with it are dispensable in milk and that its loss confers a fitness advantage.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Mobile elements facilitate genome reduction
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In the paper
“These findings imply that the Leloir Pathway is expressed at a high level during growth on plant material, which may relate to the presence of galactose in typical plant oligosaccharides like stachyose, raffinose, and melibiose.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Experimental evolution of dairy lactococci
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In the paper
“Only unambiguous SNPs with a sequence coverage of more than 20-fold and a quality score >0.99 were used for further analysis.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Genotypic characterization
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In the paper
“A rifampicin-resistant strain that showed no growth difference compared with the wild-type strain throughout the growth curve was designated KF147 RIF and used for further experiments.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Determination of relative fitness
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In the paper
“The BCAA genomic locus was shown to be non-functional in 17 tested dairy isolates (Godon et al. 1993), and pseudogenes were identified in the leucine operon of the three sequenced dairy strains IL1403, SK11, and MG1363 (Bolotin et al. 2001;Makarova et al. 2006;Wegmann et al. 2007).”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Down-regulation of BCAA biosynthesis is consistent with genome decay of dairy isolates
What the sources say
- Not checked yetcites Godon et al. 1993
- Not checked yetcites Bolotin et al. 2001
- Not checked yetcites Makarova et al. 2006
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In the paper
“The 2721 putative genes were represented by one (5.4%),two (6.7%), three to six (68%), or seven or more probes (11.7%).”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Design of microarrays
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In the paper
“Alternatively, such an increase in fitness might be limited to lactococci isolated from the plant environment, which have been described to harbor additional genes that allow them to grow in nutritionally poorer and more dynamic environments than milk (van Hylckama Vlieg et al. 2006;Siezen et al. 2008).”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Extracellular protease could not be stabilized by host-plasmid coevolution
What the sources say
- Not checked yetcites van Hylckama Vlieg et al. 2006
- Not checked yetcites Siezen et al. 2008
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In the paper
“These carbon sources are particularly abundant in plant-associated niches, and their loss or down-regulation is expected and consistent with earlier descriptions of genomic and phenotypic traits of dairy lactococci (Siezen et al. 2008).”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Genes associated with plant-polymer utilization are down-regulated in milk-adapted strains
What the sources say
- Not checked yetcites Siezen et al. 2008
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Despite the positive effects on growth rate and growth yield, the rapid loss of the protease-encoding plasmid suggests that it imposes a high burden on the cell.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Extracellular protease could not be stabilized by host-plasmid coevolution
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In the paper
“(*) Microarray probes designed to detect oppC are not 100% matching to the sequence of strain IL594-the actual expression level of oppC in strain IL594 might therefore be higher than indicated.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Array data analysis
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In the paper
“To increase the accuracy of Single Nucleotide Polymorphism (SNP) and INsertion/DELETion (INDEL) identification, the reference genome was also resequenced with the same technology and confirmed the sequence previously published for this strain (Siezen et al. 2010).”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Genotypic characterization
What the sources say
- Not checked yetcites Siezen et al. 2010
Strength:plain· not yet calibratedSingle caseTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Our finding that strain NZ5522 performs well in milk despite the low expression of the BCAA biosynthesis operon appears to falsify the first and strongly favors the second explanation.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Down-regulation of BCAA biosynthesis is consistent with genome decay of dairy isolates
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In the paper
“A total of 218 putative genes were not represented on the array because no unique probe satisfying the selection criteria could be selected.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Design of microarrays
Strength:plain· not yet calibratedCausal:direct· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Since the protease is located extracellularly, peptides produced by it will also be consumed by protease-negative cheater variants, allowing these to invade the culture.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Extracellular protease could not be stabilized by host-plasmid coevolution
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
In the paper
“The coagulation of milk was considered an indicator of fully grown cultures since lactococcal growth in milk is tightly coupled to lactic acid production and ceases after milk coagulation (Supplemental Fig. 7).”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Experimental evolution
What the sources say
- Not checked yetcites Supplemental Fig. 7
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim. It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The observation that niche-specific adaptations occurring in environmental isolates can be reproduced by experimental evolution opens exciting possibilities for the investigation of evolutionary strategies as they occur in complex environmental samples.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Conclusion
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✗ Checkable: fails✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim. It may be too vague to check against evidence.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Although clearly the averaged P-values do not represent an FDR-corrected P-value anymore, low average P-values for a gene are still indicative of highly significant regulation ratios, and, in fact, they are likely to underestimate the significance of the observed regulation.”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Array data analysis
Strength:hedged· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“Notably, also dairy adapted strains of Streptococcus thermophilus and Lactobacillus bulgaricus show high proportions of pseudogenes related to carbohydrate metabolism (Bolotin et al. 2004;van de Guchte et al. 2006).”
§ Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution > Genes associated with plant-polymer utilization are down-regulated in milk-adapted strains
What the sources say
- Not checked yetcites Bolotin et al. 2004
- Not checked yetcites van de Guchte et al. 2006
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“In this context, we cannot clearly predict the scale at which improved phenotypes emerge during laboratory evolution, although recent literature indicates that such predictions are possible in certain growth contexts such as carbon source adaptation [65].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [65]
In the citing paper
“Subsequently, it was shown that suboptimal growth on glycerol can approach its theoretical maximum during laboratory evolution [65].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [65]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
OppC and oppD deletions are assigned inconsistently
MajorThe text and Table 2 assign the adenine deletion 48 bases upstream to oppD and the thymidine deletion 64 bases upstream to oppC. Figure 3 reverses those assignments, attributing the thymidine deletion to oppD and the adenine deletion to oppC; this changes which mutation is proposed to explain increased expression.
“Remarkably, in strains NZ5521 and NZ5522, an identical single base-pair deletion of an adenine residue was identified 48 bases up-stream of the first gene in this operon (oppD) (Fig. 3; Table 2).”
“The deletion of a thymidine residue 64 bases upstream of the GTG-start codon of oppD in strains NZ5521 and NZ5522 is likely to explain the higher expression levels in these strains.In the same two strains, the deletion of an adenine residue (blue) in the upstream region of the truncated oppC gene generates an (alternative) start codon (purple)”
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Metadata
- Authors
- Bachmann, H., Starrenburg, M. J. C., Molenaar, D., Kleerebezem, M., & van Hylckama Vlieg, J. E. T.
- Affiliations
- Nederlands Instituut Voor Zuivel Oonderzoek (NL)
- Venue
- Genome Research
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2011-11-11
- Volume
- 22
- Issue
- 1
- Pages
- 115-124
- ISSN
- 1088-9051 (ISSN-L)
- PMC
- PMC3246198
- OpenAlex
- W2037362492
- Semantic Scholar
- 17f0bb98eba2f0b6aa5dde7979c0ef4add070073
- Cited by
- 170
- References
- 63
- Citations by year
- 2026: 6 · 2025: 9 · 2024: 12 · 2023: 7 · 2022: 12 · 2021: 15 · 2020: 9 · 2019: 17 · 2018: 10 · 2017: 13 · 2016: 10 · 2015: 16 · 2014: 14 · 2013: 11 · 2012: 8
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genome Research (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- VU Research Portal (publishedVersion)
- Socio-Environmental Systems Modeling (acceptedVersion)
- HighWire Press Open Archive (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- Lactococcus lactis, experimental evolution, niche adaptation, milk acidification, nitrogen metabolism, amino acid biosynthesis, genome resequencing, transcriptome, lactic acid bacteria
- MeSH terms
- Dairy Products, Lactococcus lactis, Transcription, Genetic, Gene Expression Regulation, Bacterial, Genome, Bacterial, Point Mutation, Evolution, Molecular, Genetic Loci
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