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Research Article | Host-Microbe Biology

d-Serine Degradation by Proteus mirabilis Contributes to Fitness during Single-Species and Polymicrobial Catheter-Associated Urinary Tract Infection

Aimee L. Brauer, Ashley N. White, Brian S. Learman, Alexandra O. Johnson, Chelsie E. Armbruster
Sarah E. F. D'Orazio, Editor
Aimee L. Brauer
aDepartment of Microbiology and Immunology, Jacobs School of Medicine and Biomedical Sciences, State University of New York at Buffalo, Buffalo, New York, USA
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Ashley N. White
aDepartment of Microbiology and Immunology, Jacobs School of Medicine and Biomedical Sciences, State University of New York at Buffalo, Buffalo, New York, USA
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Brian S. Learman
aDepartment of Microbiology and Immunology, Jacobs School of Medicine and Biomedical Sciences, State University of New York at Buffalo, Buffalo, New York, USA
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Alexandra O. Johnson
aDepartment of Microbiology and Immunology, Jacobs School of Medicine and Biomedical Sciences, State University of New York at Buffalo, Buffalo, New York, USA
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Chelsie E. Armbruster
aDepartment of Microbiology and Immunology, Jacobs School of Medicine and Biomedical Sciences, State University of New York at Buffalo, Buffalo, New York, USA
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  • ORCID record for Chelsie E. Armbruster
Sarah E. F. D'Orazio
University of Kentucky
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DOI: 10.1128/mSphere.00020-19
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  • FIG 1
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    FIG 1

    Proteus mirabilis can utilize d-serine as a sole source of carbon and nitrogen. Proteus mirabilis strain HI4320 was cultured in LB broth overnight and diluted 1:100 into Proteus minimal salts medium (PMSM) containing increasing concentrations of d-serine as the sole source of carbon (A) or nitrogen (B). Growth was assessed at 37°C with aeration in a 96-well plate reader by measurement of OD600 at hourly intervals for 18 h. Error bars represent means ± standard deviations (SDs) from at least 6 replicates, and graphs are representative of 4 independent experiments. The addition of ≥0.5 mM d-serine as a carbon source or ≥0.05 mM d-serine as a nitrogen source promoted significant growth as determined by paired two-way ANOVA with Dunnett’s test for multiple comparisons (P < 0.001).

  • FIG 2
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    FIG 2

    Proteus mirabilis strain HI4320 (WT) and isogenic mutants for dsdA, dsdC, or dsdX were cultured in LB broth overnight and diluted 1:100 into fresh LB (A), PMSM (B), PMSM containing 10 mM d-serine as the sole source of carbon (C), PMSM containing 10 mM d-serine as the sole source of nitrogen (D), PMSM containing 10 mM l-serine as the sole source of carbon (E), or PMSM containing 10 mM l-serine as the sole source of nitrogen (F), and growth was assessed as described in the legend for Fig. 1. Error bars represent means ± standard deviations (SDs) from at least 6 replicates, and graphs are representative of 3 independent experiments. In PMSM with d-serine as the sole source of carbon or nitrogen, the WT exhibited significantly increased growth compared to that of the mutants by paired two-way ANOVA with Dunnett’s test for multiple comparisons (P < 0.001).

  • FIG 3
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    FIG 3

    d-Serine toxicity perturbs growth of P. mirabilis in minimal medium with a rich carbon source. Proteus mirabilis strain HI4320 (WT) (A and C) and the dsdA mutant (B and D) were cultured in LB broth overnight and diluted 1:100 into the standard formulation of PMSM supplemented with 10 mM d-serine (A and B) or 10 mM d-serine and either 1 mM calcium pantothenic acid or 1 mM l-serine (C and D). Growth was assessed as described in the legend for Fig. 1. Error bars represent means ± standard deviations (SDs) with at least 6 replicates, and graphs are representative of 4 independent experiments. Visible differences in growth curves for the dsdA mutant were confirmed by paired two-way ANOVA with Dunnett’s test for multiple comparisons (P < 0.05).

  • FIG 4
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    FIG 4

    d-Serine does not provide a fitness advantage during growth in urine. Proteus mirabilis strain HI4320 (WT) and isogenic mutants for dsdA, dsdC, or dsdX were cultured in LB broth overnight and diluted 1:100 into pooled filter-sterilized urine from female humans (A to E) or female CBA/J mice (F), and incubated at 37°C with aeration for 6 h. (A) Growth of the WT and each mutant was assessed at hourly intervals by sampling independent urine cultures and plating to determine bacterial CFU/ml. Error bars represent means ± SDs from three independent experiments; no significant differences were identified by two-way ANOVA with multiple-comparison test. (B) The impact of d-serine supplementation on growth was assessed for WT and dsdA strains by adding 10 mM d-serine to urine, and growth was assessed as described above. Symbols indicate bacterial CFU/ml for one independent experiment. The relative fitness of dsdA (C), dsdC (D), and dsdX (E) mutants was determined by inoculating urine with a 1:1 mixture of mutant/WT and assessing the CFU of each at hourly intervals. A competitive index (CI) was calculated at each time point by dividing the ratio of mutant/WT for a given time point by the ratio of mutant/WT at time zero. Each symbol represents the log10 CI for one independent experiment. (F) The relative fitness of the dsdA mutant was also assessed in mouse urine, as above. Each symbol represents the log10 CI for one independent experiment, error bars represent the medians, and the dashed lines indicate log10 CI of 0 (the expected value if the ratio of mutant/WT is 1:1). No significant differences in CIs were identified by Wilcoxon signed-rank test.

  • FIG 5
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    FIG 5

    Loss of d-serine utilization does not impact P. mirabilis motility or urease activity. Proteus mirabilis strain HI4320 (WT) and isogenic mutants for dsdA, dsdC, or dsdX were cultured in LB broth overnight and stab inoculated into motility agar (A), inoculated onto the surfaces of swarm agar plates (B), or subcultured in human urine for measurement of urease activity (C). Motility diameters were measured in millimeters after 16 h of incubation at 30°C (A) or 37°C (B); error bars represent means ± SDs from three independent experiments with at least 3 replicates each. *, P < 0.05, ***, P < 0.001 by two-way ANOVA with multiple-comparison test. (C) Urease activity was measured at 30-min intervals; error bars represent means ± SDs from three independent experiments. No significant differences were identified by two-way ANOVA.

  • FIG 6
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    FIG 6

    d-Serine utilization contributes to P. mirabilis fitness in a murine model of CAUTI. Proteus mirabilis strain HI4320 (WT) and the dsdA mutant were cultured in LB broth overnight, washed once in PBS, and adjusted to 2 × 106 CFU/ml. (A) CBA/J mice were transurethrally inoculated with 50 µl of either WT (n = 10) or dsdA (n = 11) strains at 1 × 105 CFU, and a 4-mm segment of silicone catheter tubing was advanced into the bladder during inoculation. Mice were euthanized 96 h postinoculation (hpi), and bacterial burden was determined in the urine, bladders, kidneys, and spleens. Each symbol represents the log10 CFU per milliliter of urine or gram of tissue from an individual mouse, gray bars represent the medians, and the dashed line indicates the limit of detection. *, P < 0.05 by nonparametric Mann-Whitney test. (B and C) CBA/J mice (n = 11) were inoculated as described above with a 1:1 mixture of WT and dsdA strains to determine fitness during cochallenge. (B) Each symbol represents the log10 CFU per milliliter of urine or gram of tissue from an individual mouse, with the WT and dsdA CFU connected by a black line. Gray bars represent the means, and the dashed line indicates the limit of detection. (C) A competitive index was calculated as described above. Each symbol represents the log10 CI for an individual mouse, error bars represent the medians and the dashed line indicates log10 CI = 0 (the expected value if the ratio of mutant/WT is 1:1). *, P < 0.05, **, P < 0.01 by Wilcoxon signed-rank test.

  • FIG 7
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    FIG 7

    Not all uropathogens can utilize d-serine as a sole source of carbon or nitrogen. Proteus mirabilis strain HI4320 (WT), Escherichia coli strain CFT073, Providencia stuartii strain BE2467, and Morganella morganii strain TA43 were cultured in LB broth overnight and diluted 1:100 into the standard formulation of PMSM (A), PMSM containing 10 mM d-serine as the sole carbon source (B), and PMSM containing 10 mM d-serine as the sole nitrogen source (C). Growth was assessed as described above. Error bars represent means ± standard deviations (SD) from 3 experiments with at least 6 replicates each. Growth of P. stuartii was significantly lower than each of the other species in panels B and C as determined by paired two-way ANOVA with Dunnett’s test for multiple comparisons (P < 0.05).

  • FIG 8
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    FIG 8

    Not all uropathogens degrade d-serine during growth in human urine. Proteus mirabilis strain HI4320 (WT), E. coli CFT073 (Ec), M. morganii TA43 (Mm), and P. stuartii BE2467 (Ps) were cultured in LB broth overnight and E. faecalis 3143 (Ef) was cultured in BHI overnight. Overnight cultures were diluted 1:100 into pooled filter-sterilized urine from female donors that had been diluted 1:1 with sterile saline and incubated for 18 h at 37°C with aeration, and d- and l-serine were quantified using a fluorometric detection kit for comparison to the starting urine pool. Bars represent total serine concentration, divided into d-serine and l-serine for three independent replicates. ns, P > 0.05, ***, P < 0.001 by two-way ANOVA.

  • FIG 9
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    FIG 9

    d-Serine utilization provides a fitness advantage to P. mirabilis during polymicrobial CAUTI. Proteus mirabilis strain HI4320 (WT), the dsdA mutant (dsdA), E. coli CFT073 (Ec), P. stuartii BE2467 (Ps), and M. morganii TA43 (Mm) were cultured in LB broth overnight, and E. faecalis 3143 (Ef) was cultured in BHI overnight. All cultures were washed once in PBS and adjusted to 2 × 106 CFU/ml. CBA/J mice were transurethrally inoculated with 50 µl of a mixture containing 5 × 104 CFU of a 1:1 mixture of dsdA and WT P. mirabilis and 5 × 104 CFU of either E. coli CFT073 (A and B,; n = 8), M. morganii TA43 (C and D; n = 7), P. stuartii BE2467 (E and F; n = 8), or E. faecalis 3143 (G and H; n = 7). A 4-mm segment of silicone catheter tubing was advanced into the bladder during inoculation, and mice were euthanized 96 h postinoculation (hpi) for determination of bacterial burden in the urine, bladders, kidneys, and spleens. (A, C, E, and G) Each symbol represents the log10 CFU per milliliter of urine or gram of tissue recovered from an individual mouse, connected by black lines: triangles represent the coinfecting species, black circles represent the WT P. mirabilis, and open blue circles represent the dsdA mutant. Gray bars represent the means, and the dashed lines indicate the limits of detection. (B, D, F, and H) Each symbol represents the log10 CI for the dsdA mutant recovered from an individual mouse for which CFU were above the limit of detection, error bars represent the medians and the dashed lines indicate log10 CI = 0 (the expected value if the ratio of mutant/WT is 1:1). *, P < 0.05, **, P < 0.01 by Wilcoxon signed-rank test.

  • FIG 10
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    FIG 10

    d-Serine utilization contributes to fitness of P. mirabilis within the bloodstream. Proteus mirabilis strain HI4320 (WT, black circles) and the dsdA mutant (open blue circles) were cultured in LB broth overnight, washed once in PBS, and adjusted to 2 × 108 CFU/ml. CBA/J mice (n = 8) were inoculated by tail vein injection of 100 µl containing a 1:1 mixture of dsdA and WT strains. Mice were euthanized at 24 hpi, and bacterial burden was determined in the spleens, livers, and kidneys. (A) Each symbol represents the log10 CFU per gram of tissue from an individual mouse, with the WT and dsdA CFU connected by black lines. Gray bars represent the means, and the dashed line indicates the limit of detection. (B) A competitive index was calculated as described above. Each symbol represents the log10 CI for an individual mouse, error bars represent the medians, and the dashed line indicates log10 CI = 0 (the expected value if the ratio of mutant/WT is 1:1). *, P < 0.05, **, P < 0.01 by Wilcoxon signed-rank test.

Supplemental Material

  • Figures
  • FIG S1

    dsdA is required for growth of P. mirabilis when d-serine is the sole carbon or nitrogen source. Proteus mirabilis strain HI4320 (WT) and the dsdA mutant were cultured in LB broth overnight, diluted 1:100 into PMSM with 10 mM d-serine as the sole source of carbon or nitrogen, and incubated at 37°C with aeration for 24 h. An aliquot was taken at the start of the culture, at 3 h, and at 24 h to assess viability by plating on LB agar for determination of log10 CFU/ml. Error bars represent means ± SDs from three independent experiments. Download FIG S1, TIF file, 0.2 MB.

    Copyright © 2019 Brauer et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S2

    d-Serine utilization defects can be partially complemented. Proteus mirabilis strain HI4320 (WT) harboring pGEN-MCS, the dsdA mutant harboring pGEN-MCS, and the dsdA mutant complemented with the WT dsdA gene on pGEN-dsdA were cultured in LB broth with ampicillin overnight and diluted 1:100 into PMSM containing 10 mM d-serine as the sole source of carbon (A) or nitrogen (B). Growth was assessed at 37°C in a 96-well plate reader by measurement of OD600 at hourly intervals for 18 h. Error bars represent means ± standard deviations (SDs) from two independent experiments with 6 replicates each. The complemented dsdA strain exhibited significantly increased growth under both conditions compared to that of the dsdA strain harboring pGEN-MCS by paired two-way ANOVA with Dunnett’s test for multiple comparisons (P < 0.05). However, growth was not complemented to the level observed for the WT. Download FIG S2, TIF file, 0.4 MB.

    Copyright © 2019 Brauer et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S1

    BLAST comparison of dsdA among P. mirabilis genomes. Download Table S1, XLSX file, 0.1 MB.

    Copyright © 2019 Brauer et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S2

    BLAST comparison of dsdX among P. mirabilis genomes. Download Table S2, XLSX file, 0.1 MB.

    Copyright © 2019 Brauer et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S3

    d-Serine degradation is common among P. mirabilis clinical isolates. Fourteen Proteus mirabilis clinical isolates were cultured in LB broth overnight and diluted 1:100 into PMSM minimal medium containing 10 mM d-serine as the sole source of nitrogen. Growth was assessed at 37°C in a 96-well plate reader by measurement of OD600 at hourly intervals for 18 h, and P. mirabilis strain HI4320 and the dsdA mutant were included for comparison. Error bars represent means ± standard deviations (SDs) from two independent experiments with 6 replicates each. All fourteen strains were capable of growing on d-serine as the sole source of nitrogen, indicative of d-serine degradation. Download FIG S3, TIF file, 0.6 MB.

    Copyright © 2019 Brauer et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S4

    Proteus mirabilis strain HI4320 (WT) and isogenic mutants for dsdA, dsdC, or dsdX were cultured in LB broth overnight and diluted 1:100 into the standard formulation of PMSM supplemented with either 10 mM d-serine (A) or 10 mM l-serine (B). Growth was assessed as described above. Error bars represent means ± standard deviations (SDs) with at least 6 replicates, and graphs are representative of at least 2 experiments. Download FIG S4, TIF file, 0.6 MB.

    Copyright © 2019 Brauer et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S5

    Proteus mirabilis strain HI4320 (WT) harboring pGEN-MCS, the dsdA mutant harboring pGEN-MCS, and the dsdA mutant complemented with the WT dsdA gene on pGEN-dsdA were cultured in LB broth with ampicillin overnight and diluted 1:100 into the standard formulation of PMSM supplemented with 10 mM d-serine. Growth was assessed as described above. Error bars represent means ± standard deviations (SDs) from 2 independent experiments with 6 replicates each. Download FIG S5, TIF file, 0.2 MB.

    Copyright © 2019 Brauer et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S3

    BLAST comparison of dsdA among M. morganii genomes. Download Table S3, XLSX file, 0.1 MB.

    Copyright © 2019 Brauer et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S4

    BLAST comparison of dsdA among E. faecalis genomes. Download Table S4, XLSX file, 0.1 MB.

    Copyright © 2019 Brauer et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S5

    BLAST comparison of dsdA among P. stuartii genomes. Download Table S5, XLSX file, 0.1 MB.

    Copyright © 2019 Brauer et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

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d-Serine Degradation by Proteus mirabilis Contributes to Fitness during Single-Species and Polymicrobial Catheter-Associated Urinary Tract Infection
Aimee L. Brauer, Ashley N. White, Brian S. Learman, Alexandra O. Johnson, Chelsie E. Armbruster
mSphere Feb 2019, 4 (1) e00020-19; DOI: 10.1128/mSphere.00020-19

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d-Serine Degradation by Proteus mirabilis Contributes to Fitness during Single-Species and Polymicrobial Catheter-Associated Urinary Tract Infection
Aimee L. Brauer, Ashley N. White, Brian S. Learman, Alexandra O. Johnson, Chelsie E. Armbruster
mSphere Feb 2019, 4 (1) e00020-19; DOI: 10.1128/mSphere.00020-19
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KEYWORDS

d-amino acid
Enterococcus faecalis
Escherichia coli
Morganella morganii
Proteus mirabilis
Providencia stuartii
bacteremia
catheter
polymicrobial
serine
urinary tract
urine

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