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Machine-learning from Pseudomonas putida KT2440 transcriptomes reveals its transcriptional regulatory network

Lim, Hyun Gyu, Rychel, Kevin, Sastry, Anand V., Bentley, Gayle J., Mueller, Joshua, Schindel, Heidi S., Larsen, Peter E., Laible, Philip D., Guss, Adam M., Niu, Wei, Johnson, Christopher W., Beckham, Gregg T., Feist, Adam M., Palsson, Bernhard O.·2022·Metabolic Engineering
DOI 10.1016/j.ymben.2022.04.004

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Fig. 1 Independent component analysis (ICA) of the putida PRECISE321 transcriptome compendium. (a) Overall data processing pipeline for independent component analysis (ICA) of putida PRECISE321. By performing ICA, the gene expression profiles [X] (5564 genes by 321 conditions) were deconvoluted into an [M] matrix containing weights of 5564 genes for each of the 84 iModulon identified, and an [A] matrix containing iModulon activities for each condition. A part of this diagram was adapted from Sastry et al. (2021). (b) A treemap of P. putida ' s 84 iModulons. The size of each rectangle indicates the explained variances in the data sets attributable to each iModulon. (c) Bottom-up vs top-down assessment of co-regulated genes (i.e, bio-molecular vs data-driven). The scatter plot shows Regulon Recalls (RR) and iModulon Recalls (IR) for 39 regulatory iModulons. For iModulons with names consisting of two regulators, RR and IR are the values of the first regulator. Colors indicate iModulon types. (d) An example of a well-matched case: HexR. Gene weights of the HexR iModulon. (e) Condition-dependent HexR iModulon activities with the supplementation of different carbon sources. Asterisks indicate the reference conditions (glucose minimal media). It should be noted that each project (separated by gray lines) was normalized to its unique control condition (Supplementary Data) to remove batch effects, so activity values from different projects should not be directly compared. (f) Enriched motif (top) from the upstream of HexR-regulating genes and previously reported HexR binding site (bottom, obtained from CollectTF (Kiliç et al., 2014)).
Fig. 1 Independent component analysis (ICA) of the putida PRECISE321 transcriptome compendium. (a) Overall data processing pipeline for independent component analysis (ICA) of putida PRECISE321. By performing ICA, the gene expression profiles [X] (5564 genes by 321 conditions) were deconvoluted into an [M] matrix containing weights of 5564 genes for each of the 84 iModulon identified, and an [A] matrix containing iModulon activities for each condition. A part of this diagram was adapted from Sastry et al. (2021). (b) A treemap of P. putida ' s 84 iModulons. The size of each rectangle indicates the explained variances in the data sets attributable to each iModulon. (c) Bottom-up vs top-down assessment of co-regulated genes (i.e, bio-molecular vs data-driven). The scatter plot shows Regulon Recalls (RR) and iModulon Recalls (IR) for 39 regulatory iModulons. For iModulons with names consisting of two regulators, RR and IR are the values of the first regulator. Colors indicate iModulon types. (d) An example of a well-matched case: HexR. Gene weights of the HexR iModulon. (e) Condition-dependent HexR iModulon activities with the supplementation of different carbon sources. Asterisks indicate the reference conditions (glucose minimal media). It should be noted that each project (separated by gray lines) was normalized to its unique control condition (Supplementary Data) to remove batch effects, so activity values from different projects should not be directly compared. (f) Enriched motif (top) from the upstream of HexR-regulating genes and previously reported HexR binding site (bottom, obtained from CollectTF (Kiliç et al., 2014)).CC-BY · From the PDF
Fig. 2 iModulons allow data-driven curation of the TRN in P. putida . (a-d) Characteristics of the FleQ regulon subset iModulons. (a) A Venn diagram of the two FleQ iModulons, FleQ/Fur and FleQ/AmrZ, and the FleQ regulon. (b) An activity plot of the FleQ/Fur iModulon in selected conditions. (c) Comparison of a motif found in the upstream regions of the FleQ/Fur iModulon genes and previously known binding motifs of Fur in E. coli (obtained from CollectTF (Kiliç et al., 2014)). The common motif was enriched from 25 out of 27 TUs (94.4% of the genes) in the FleQ/Fur iModulon. (d) A scatter plot of activities of the FleQ/Fur and FleQ/AmrZ iModulons for all conditions. The Pearson correlation of the two iModulon activities was 0.12. Selected samples with high activities were colored and growth conditions were indicated in the inset. Activities of the FleQ/AmrZ iModulon changed when fl eQ was deleted or an excess amount of NaCl was added. (e -h) Characteristics of the Zur regulon discovery iModulon. (e) A Venn diagram of the Zur iModulon and related Zur regulon. (f) An activity plot of the Zur iModulon in selected conditions. High activities of the Zur iModulon were observed when zinc ion or nanomaterial was added. The CJ522 strain is an engineered P. putida KT2440 strain Δ catRBCA ::Ptac: catA Δ pcaHG ::Ptac: aroY : ecdB : asbF Δ pykA :: aroG D146N : aroY : ecdB : asbF Δ pykF Δ ppc Δ pgi -1 Δ pgi -2 Δ gcd (Johnson et al., 2019). (g) Comparison with an enriched motif from 11 TUs in the Zur iModulon (66.7% of the total genes) and a previously reported P. protegens Pf-5 Zur binding motif (obtained from CollectTF (Kiliç et al., 2014)). (h) A schematic diagram of regulation by Zur. Previously known regulations were colored in black while newly predicted regulations were colored in red. Potential indirect regulations were indicated with dashed gray lines. (i -l) Characteristics of the PP_0204 poorly-matched iModulon. (i) A Venn diagram of the PP_0204/CysB iModulon and PP_0204 regulon. (j) An activity plot of the PP_0204 iModulon in selected conditions. Asterisks indicate the reference conditions. (k) Comparison with an enriched motif from 11 TUs in the PP_0204 iModulon and an enriched motif from 14 TUs in the E. coli CysB regulon (obtained from RegulonDB (Santos-Zavaleta et al., 2019)) (l) Gene weight correlation of the PP_0204/CysB iModulon and the Cbl + CysB iModulon of E. coli. The dashed lines indicate the threshold values (0.054 and 0.075) for E. coli and P. putida to determine iModulon member genes. See Methods for the calculation. (a, e, and i) Gene numbers were shown in these diagrams. (b, f, and j) Asterisks indicate the reference conditions.
Fig. 2 iModulons allow data-driven curation of the TRN in P. putida . (a-d) Characteristics of the FleQ regulon subset iModulons. (a) A Venn diagram of the two FleQ iModulons, FleQ/Fur and FleQ/AmrZ, and the FleQ regulon. (b) An activity plot of the FleQ/Fur iModulon in selected conditions. (c) Comparison of a motif found in the upstream regions of the FleQ/Fur iModulon genes and previously known binding motifs of Fur in E. coli (obtained from CollectTF (Kiliç et al., 2014)). The common motif was enriched from 25 out of 27 TUs (94.4% of the genes) in the FleQ/Fur iModulon. (d) A scatter plot of activities of the FleQ/Fur and FleQ/AmrZ iModulons for all conditions. The Pearson correlation of the two iModulon activities was 0.12. Selected samples with high activities were colored and growth conditions were indicated in the inset. Activities of the FleQ/AmrZ iModulon changed when fl eQ was deleted or an excess amount of NaCl was added. (e -h) Characteristics of the Zur regulon discovery iModulon. (e) A Venn diagram of the Zur iModulon and related Zur regulon. (f) An activity plot of the Zur iModulon in selected conditions. High activities of the Zur iModulon were observed when zinc ion or nanomaterial was added. The CJ522 strain is an engineered P. putida KT2440 strain Δ catRBCA ::Ptac: catA Δ pcaHG ::Ptac: aroY : ecdB : asbF Δ pykA :: aroG D146N : aroY : ecdB : asbF Δ pykF Δ ppc Δ pgi -1 Δ pgi -2 Δ gcd (Johnson et al., 2019). (g) Comparison with an enriched motif from 11 TUs in the Zur iModulon (66.7% of the total genes) and a previously reported P. protegens Pf-5 Zur binding motif (obtained from CollectTF (Kiliç et al., 2014)). (h) A schematic diagram of regulation by Zur. Previously known regulations were colored in black while newly predicted regulations were colored in red. Potential indirect regulations were indicated with dashed gray lines. (i -l) Characteristics of the PP_0204 poorly-matched iModulon. (i) A Venn diagram of the PP_0204/CysB iModulon and PP_0204 regulon. (j) An activity plot of the PP_0204 iModulon in selected conditions. Asterisks indicate the reference conditions. (k) Comparison with an enriched motif from 11 TUs in the PP_0204 iModulon and an enriched motif from 14 TUs in the E. coli CysB regulon (obtained from RegulonDB (Santos-Zavaleta et al., 2019)) (l) Gene weight correlation of the PP_0204/CysB iModulon and the Cbl + CysB iModulon of E. coli. The dashed lines indicate the threshold values (0.054 and 0.075) for E. coli and P. putida to determine iModulon member genes. See Methods for the calculation. (a, e, and i) Gene numbers were shown in these diagrams. (b, f, and j) Asterisks indicate the reference conditions.CC-BY · From the PDF
Fig. 3 iModulons describe global transcriptional changes after the transition from the growth phase to the stationary phase. (a) Differentially changed iModulon activities during the transition from the exponential growth phase to the stationary phase at a threshold of 5 and an FDR of 0.05. Unexpected changes were colored in purple. (b) Activities of the PydR/RpoS and Translation iModulons in selected samples. Project names are colored in gray. Asterisks indicate the reference conditions for each project. (c) Activity correlation of the PydR/RpoS and Translation iModulons. Activity of these two iModulons showed a negative correlation across samples (Pearson correlation coefficient R of 0.58, p -value < 1 × 10 10 ).
Fig. 3 iModulons describe global transcriptional changes after the transition from the growth phase to the stationary phase. (a) Differentially changed iModulon activities during the transition from the exponential growth phase to the stationary phase at a threshold of 5 and an FDR of 0.05. Unexpected changes were colored in purple. (b) Activities of the PydR/RpoS and Translation iModulons in selected samples. Project names are colored in gray. Asterisks indicate the reference conditions for each project. (c) Activity correlation of the PydR/RpoS and Translation iModulons. Activity of these two iModulons showed a negative correlation across samples (Pearson correlation coefficient R of 0.58, p -value < 1 × 10 10 ).CC-BY · From the PDF
Fig. 4 iModulons show transcriptional responses to the utilization of different substrates. (a) Metabolic pathway associated with iModulons for substrate utilization in P. putida . Boundaries of iModulons (names in red) were indicated by colored rounded shapes. Names of genes belonging to iModulons were colored in black. Subcellular localization information was obtained from Pseudomonas.com (Winsor et al., 2016). (b) Activities of the carbon utilization iModulons depending on substrates. For a clear comparison, the minimum and maximum activity values were set to 15 and 15, respectively. (c) The activities of the 22 iModulons, that showed differential activities during the transition to the stationary phase from the growth phase, during utilization of each substrate. For clear visualization, the minimum and maximum activities were set to 25 and 25, respectively. (b and c) Multiple RNA-Seq samples with the same substrates were differentiated by adding numbers. iModulon activities in the glucose condition are zero. (d) A scatter plot of the growth rates and Pearson correlation coefficients of activities of the ' sta­ tionary response ' in iModulons in the group. Abbreviations: GAL, galactose; GLC, glucose; GLCN, gluconate; XYL, xylose; ACE, acetate; MA, myristic acid; CIT, citrate; FRU, fructose; SER, serine; 2-KG, 2-ketogluconate; XYLNT, xylonate; 2K3DXT, 2-keto-3-deoxyxylonate; 2KGSA, 2-keto-glutaric semialdehyde; G6P, glucose-6-phosphate (P); 6 PG, 6-phosphogluconate; 2KG6P, 2-ketogluconate-6-P; Gal1P, galactose-1-P; F-1-P, fructose-1-P; UDP-Glc, uridine diphosphate-glucose; UDP-Gal, uridine diphosphate galactose; G1P, glucose-1-P; KDPG, 2-dehydro-3-deoxy-phosphogluconate; PYR, pyruvate; G3P, glyceraldehyde-3-P; 3 PG, glycerate-3-P; 2 PG, 2-phosphoglycerate; PEP, phosphoenolpyruvate; acetyl-CoA, acetyl coenzyme A (CoA), CIT, citrate; ICT, isocitrate; α KG, α -ketoglutarate; SUC-CoA, succinyl-CoA; SUC, succinate; FUM, fumarate; MAL, malate; OAA, oxaloacetate; GLY, glyoxylate.
Fig. 4 iModulons show transcriptional responses to the utilization of different substrates. (a) Metabolic pathway associated with iModulons for substrate utilization in P. putida . Boundaries of iModulons (names in red) were indicated by colored rounded shapes. Names of genes belonging to iModulons were colored in black. Subcellular localization information was obtained from Pseudomonas.com (Winsor et al., 2016). (b) Activities of the carbon utilization iModulons depending on substrates. For a clear comparison, the minimum and maximum activity values were set to 15 and 15, respectively. (c) The activities of the 22 iModulons, that showed differential activities during the transition to the stationary phase from the growth phase, during utilization of each substrate. For clear visualization, the minimum and maximum activities were set to 25 and 25, respectively. (b and c) Multiple RNA-Seq samples with the same substrates were differentiated by adding numbers. iModulon activities in the glucose condition are zero. (d) A scatter plot of the growth rates and Pearson correlation coefficients of activities of the ' sta­ tionary response ' in iModulons in the group. Abbreviations: GAL, galactose; GLC, glucose; GLCN, gluconate; XYL, xylose; ACE, acetate; MA, myristic acid; CIT, citrate; FRU, fructose; SER, serine; 2-KG, 2-ketogluconate; XYLNT, xylonate; 2K3DXT, 2-keto-3-deoxyxylonate; 2KGSA, 2-keto-glutaric semialdehyde; G6P, glucose-6-phosphate (P); 6 PG, 6-phosphogluconate; 2KG6P, 2-ketogluconate-6-P; Gal1P, galactose-1-P; F-1-P, fructose-1-P; UDP-Glc, uridine diphosphate-glucose; UDP-Gal, uridine diphosphate galactose; G1P, glucose-1-P; KDPG, 2-dehydro-3-deoxy-phosphogluconate; PYR, pyruvate; G3P, glyceraldehyde-3-P; 3 PG, glycerate-3-P; 2 PG, 2-phosphoglycerate; PEP, phosphoenolpyruvate; acetyl-CoA, acetyl coenzyme A (CoA), CIT, citrate; ICT, isocitrate; α KG, α -ketoglutarate; SUC-CoA, succinyl-CoA; SUC, succinate; FUM, fumarate; MAL, malate; OAA, oxaloacetate; GLY, glyoxylate.CC-BY · From the PDF
Fig. 5 Analyzing iModulon activities unveil evolutionary strategies to achieve high fitness in a glucose minimal medium condition. (a) Mutations identified in the wildtype, A1_F11_I1 (early1), A1_F84_I1 (end1), A2_F83_I1 (end2), A3_F85_I1 (end3), and A4_F88_I1 (end4) strains (Lim et al., 2020). Strain names indicate passage numbers during an evolution study (see Supplementary Note 3). Colors: orange, single amino acid changes or an in-frame deletion; green, nonsynonymous mutation; red, early termination or frame-shift mutations (b) Maximum specific rates (h 1 ) of the six strains in a glucose minimal medium. (c) Differential iModulon activity plot for the A1_F11_I1 and wildtype strains. (d and e) Differential iModulon activity plot for the A1_F11_I1 versus either (d) A3_F85_I1 or (e) A4_F88_I1 strain. iModulon activities in the non-wild type strains were inferred from the [M] matrix of the original iModulon activity. Dashed gray lines indicate a threshold value of 5 and solid gray lines indicate a 45-degree line of each plot. Null iModulons were colored in gray even with changes greater than 5.
Fig. 5 Analyzing iModulon activities unveil evolutionary strategies to achieve high fitness in a glucose minimal medium condition. (a) Mutations identified in the wildtype, A1_F11_I1 (early1), A1_F84_I1 (end1), A2_F83_I1 (end2), A3_F85_I1 (end3), and A4_F88_I1 (end4) strains (Lim et al., 2020). Strain names indicate passage numbers during an evolution study (see Supplementary Note 3). Colors: orange, single amino acid changes or an in-frame deletion; green, nonsynonymous mutation; red, early termination or frame-shift mutations (b) Maximum specific rates (h 1 ) of the six strains in a glucose minimal medium. (c) Differential iModulon activity plot for the A1_F11_I1 and wildtype strains. (d and e) Differential iModulon activity plot for the A1_F11_I1 versus either (d) A3_F85_I1 or (e) A4_F88_I1 strain. iModulon activities in the non-wild type strains were inferred from the [M] matrix of the original iModulon activity. Dashed gray lines indicate a threshold value of 5 and solid gray lines indicate a 45-degree line of each plot. Null iModulons were colored in gray even with changes greater than 5.CC-BY · From the PDF
Fig. 6 Coordinated iModulon activity changes underlie the activation of the Type VI secretion system by osmotic stress and define a stimulon. (a) Activity cor­ relation of the T6SS, Osmotic stress-1, Osmotic stress-2, and AmrZ iModulons. Activities of all these four iModulons showed a positive correlation. Font colors indicate Pearson correlation coefficients. Samples displaying high activities were colored: pink (fuel:butanol); green (fuel:isopentanol), orange (ALE:IL_TEA_HS), brown (multistress:NaCl_60min), red (mobile_genes:2737_reg-w/mobile genes at the regrowth phase), and purple (mobile_genes:3227_reg-w/mobile genes at the regrowth phase). Dashed lines are the best fits on each plot. (b) Gene weights of the T6SS iModulon. The dashed line indicates a threshold value of 0.11 (See Methods). (c) T6SS iModulon activities in selected samples from projects: mobile genes and multistress (Bojanovi ˇ c et al., 2017). See Supplementary Data for details of the experimental conditions. Asterisks indicate the reference conditions.
Fig. 6 Coordinated iModulon activity changes underlie the activation of the Type VI secretion system by osmotic stress and define a stimulon. (a) Activity cor­ relation of the T6SS, Osmotic stress-1, Osmotic stress-2, and AmrZ iModulons. Activities of all these four iModulons showed a positive correlation. Font colors indicate Pearson correlation coefficients. Samples displaying high activities were colored: pink (fuel:butanol); green (fuel:isopentanol), orange (ALE:IL_TEA_HS), brown (multistress:NaCl_60min), red (mobile_genes:2737_reg-w/mobile genes at the regrowth phase), and purple (mobile_genes:3227_reg-w/mobile genes at the regrowth phase). Dashed lines are the best fits on each plot. (b) Gene weights of the T6SS iModulon. The dashed line indicates a threshold value of 0.11 (See Methods). (c) T6SS iModulon activities in selected samples from projects: mobile genes and multistress (Bojanovi ˇ c et al., 2017). See Supplementary Data for details of the experimental conditions. Asterisks indicate the reference conditions.CC-BY · From the PDF

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Metadata

Authors
Lim, H. G., Rychel, K., Sastry, A. V., Bentley, G. J., Mueller, J., Schindel, H. S., Larsen, P. E., Laible, P. D., Guss, A. M., Niu, W., Johnson, C. W., Beckham, G. T., Feist, A. M., & Palsson, B. O.
Venue
Metabolic Engineering
Publisher
Elsevier BV
Published
2022-07
Volume
72
Pages
297-310
ISSN
1096-7176
DOI
10.1016/j.ymben.2022.04.004
Cited by
80
References
2
Language
en
Licence
Funders
  • Office of Energy Efficiency and Renewable Energy (DE-AC36-08GO28308)
  • University of Nebraska-Lincoln Nebraska Center for Energy Sciences Research
  • US Department of Energy Office of Science (DE-AC02-05CH11231, DE-AC05-00OR22725)
  • Biological and Environmental Research
  • U.S. Department of Energy
  • Bioenergy Technologies Office
  • National Renewable Energy Laboratory

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