Pathogenic Leptospires Modulate Protein Expression and Post-translational Modifications in Response to Mammalian Host Signals.

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Reservoir hosts of leptospirosis, including rodents, dogs, and cattle, exhibit little to no signs of disease but shed large numbers of organisms in their urine. Transmission occurs when mucosal surfaces or abraded skin come into contact with infected urine or urine-contaminated water or soil. Whilst little is known about how Leptospira adapt to and persist within a reservoir host, in vitro studies suggest that leptospires alter their transcriptomic and proteomic profiles in response to environmental signals encountered during mammalian infection. We applied the dialysis membrane chamber (DMC) peritoneal implant model to compare the whole cell proteome of in vivo derived leptospires with that of leptospires cultivated in vitro at 30°C and 37°C by 2-dimensional difference in-gel electrophoresis (2-D DIGE). Of 1,735 protein spots aligned across 9 2-D DIGE gels, 202 protein spots were differentially expressed (p < 0.05, fold change >1.25 or < -1.25) across all three conditions. Differentially expressed proteins were excised for identification by mass spectrometry. Data are available via ProteomeXchange with identifier PXD006995. The greatest differences were detected when DMC-cultivated leptospires were compared with IV30- or IV37-cultivated leptospires, including the increased expression of multiple isoforms of Loa22, a known virulence factor. Unexpectedly, 20 protein isoforms of LipL32 and 7 isoforms of LipL41 were uniformly identified by DIGE as differentially expressed, suggesting that unique post-translational modifications (PTMs) are operative in response to mammalian host conditions. To test this hypothesis, a rat model of persistent renal colonization was used to isolate leptospires directly from the urine of experimentally infected rats. Comparison of urinary derived leptospires to IV30 leptospires by 2-D immunoblotting confirmed that modification of proteins with trimethyllysine and acetyllysine occurs to a different degree in response to mammalian host signals encountered during persistent renal colonization. These results provide novel insights into differential protein and PTMs present in response to mammalian host signals which can be used to further define the unique equilibrium that exists between pathogenic leptospires and their reservoir host of infection.", "claims": [{"id": "claim-method", "statement": "Statistically significantly expressed protein spots were defined as having a t-test p < 0.05 and a fold change of >1.25 or < −1.25 (Supplementary Table 1).", "kind": "methodological", "target": null, "evidence": [{"asset": "source:pmid:28848720", "locator": "sections[7] \"Image acquisition and analysis\" paragraph 2", "quote": "Statistically significantly expressed protein spots were defined as having a t-test p < 0.05 and a fold change of >1.25 or < −1.25 (Supplementary Table 1)."}], "state": "complete"}, {"id": "claim-data-access", "statement": "Data are available via ProteomeXchange with identifier PXD006995.", "kind": "methodological", "target": null, "evidence": [{"asset": "source:pmid:28848720", "locator": "sections[0] \"Abstract\" paragraph 1", "quote": "Data are available via ProteomeXchange with identifier PXD006995."}], "state": "complete"}, {"id": "claim-target-result", "statement": "Using 2-D DIGE with a t-test threshold of p < 0.05 and fold change >1.25 or <−1.25, the study found 202 of 1,735 aligned protein spots differentially expressed, and the proteomics data are available through ProteomeXchange under identifier PXD006995.", "kind": "quantitative", "target": {"value": 0.05, "unit": "p-value", "tolerance": null, "source": "Of 1,735 protein spots aligned across 9 2-D DIGE gels, 202 protein spots were differentially expressed (p < 0.05, fold change >1.25 or < −1.25) across all three conditions."}, "evidence": [{"asset": "source:pmid:28848720", "locator": "sections[0] \"Abstract\" paragraph 1", "quote": "Of 1,735 protein spots aligned across 9 2-D DIGE gels, 202 protein spots were differentially expressed (p < 0.05, fold change >1.25 or < −1.25) across all three conditions."}, {"asset": "source:pmid:28848720", "locator": "sections[0] \"Abstract\" paragraph 1", "quote": "Data are available via ProteomeXchange with identifier PXD006995."}], "state": "complete"}], "gaps": []}, "experiment": {"state": "complete", "objective": "Using 2-D DIGE with a t-test threshold of p < 0.05 and fold change >1.25 or <−1.25, the study found 202 of 1,735 aligned protein spots differentially expressed, and the proteomics data are available through ProteomeXchange under identifier PXD006995.", "steps": [{"id": "read_published_estimate", "order": 1, "name": "Read the published estimate from the source", "kind": "other", "state": "complete", "blocked_on": null, "description": "The claim, method and evidence span published with the source article.", "duration_hours": null, "parameters": {}, "inputs": ["source:pmid:28848720"], "outputs": ["the published estimate and its evidence"], "instruments": [], "reagents": []}, {"id": "obtain_source_data", "order": 2, "name": "Obtain the source data from the named repository", "kind": "data-preparation", "state": "complete", "blocked_on": null, "description": "The GEO series accession resolves and its sample accessions are listed. 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(Locus tag)", "InterPro scan analysis (for proteins of unknown function)"], ["313", "0.00057", "7.05", "gi|45602612(AAS72087.1)", "methylmalonyl-CoA mutase(LIC_20058)", ""], ["992, 987", "0.000076, 0.000011", "4.49, 3.71", "gi|45601096(AAS70579.1)", "succinate dehydrogenase iron-sulfur subunit(LIC_12003)", ""], ["375, 383, 379", "0.0012, 0.017, 0.0015", "3.95, 2.59, 2.48", "gi|45600451(AAS69936.1)", "GroEL(LIC_11335)", ""], ["1,028", "0.0046", "3.53", "gi|45602037(AAS71516.1)", "LipL41(LIC_12966)", "Tetratricopeptide repeat (TPR) domain"], ["1,164", "0.013", "3.09", "gi|45601580(AAS71060.1)", "3-hydroxybutyryl-CoA dehydratase(LIC_12495)", ""], ["282, 284", "0.00071, 0.011", "2.78, 2.07", "gi|45599657(AAS69145.1)", "DnaK(LIC_10524)", ""], ["1,446, 1445", "0.0052, 0.045", "2.4, 1.75", "gi|45600006(AAS69493.1)", "putative lipoprotein(LIC_10879)", "None predicted"], ["518", "0.039", "2.02", "gi|45601495(AAS70976.1)", "putative glutamine synthetase protein(LIC_12407)", ""], ["1,318, 1,275, 1,293, 1,289", "0.0037, 0.0098, 0.026, 0.024", "1.9, 1.75, 1.58, 1.44", "gi|45599329(AAS68819.1)", "Loa 22 (peptidoglycan associated cytoplasmic membrane protein)(LIC_10191)", "OmpA-like domain"]], "row_count": 10, "column_count": 6, "numeric_cells": 45, "header_rows": 1, "locator": "section[12]/table-wrap[1]#T2"}}, {"id": "asset:table:pmid:28848720:3", "role": "table", "format": "jats-table", "media_type": "application/vnd.jats.table+json", "uri": null, "sha256": "sha256:50ca65419e9bec594c97e7474e79f612ae3008ce6eed196b423824b355cd73d5", "bytes": 4852, "access": "open", "state": "verified", "reader": "read_table", "reader_status": "available", "identifier": "section[12]/table-wrap[2]#T3", "version": null, "note": "Proteins less abundant (p < 0.05, fold > −1.25) in DMC-cultivated leptospires compared to IV30-cultivated leptospires.", "structure": {"pmcid": "PMC5553009", "section_index": 12, "section_title": "Protein identification", "row_count": 35, "column_count": 6}, "table": {"label": "Table 3", "caption": "Proteins less abundant (p < 0.05, fold > −1.25) in DMC-cultivated leptospires compared to IV30-cultivated leptospires.", "rows": [["Protein spot number", "p-value", "Av. Ratio", "GI Accession number (Accession number)", "Protein name (Locus Tag)", "InterPro scan analysis (for proteins of unknown function)"], ["1,638, 1,637", "9.3E-07, 1.1E-07", "−12.5, −9.45", "gi|45600452(AAS69937.1)", "GroES(LIC_11336)", ""], ["591, 583", "5.6E-07, 0.00022", "−10.7, −2.81", "gi|45601949(AAS71428.1)", "Elongation factor Tu(LIC_12875)", ""], ["1,266, 1,263, 1,262", "1.9E-07, 0.00021, 0.0099", "−9.25, −2.47, −1.8", "gi|45600339(AAS69825.1)", "Peroxiredoxin(LIC_11219)", ""], ["631", "1.2E-06", "−8.01", "gi|45600988(AAS70471.1)", "Putative lipoprotein (LipL46)(LIC_11885)", "None predicted"], ["1,042, 1,049", "0.000026, 0.000072", "−6.47, −5.23", "gi|45599498(AAS68987.1)", "Electron transport flavoprotein beta subunit(LIC_10361)", ""], ["633, 630, 672, 676", "0.00014, 0.00022, 0.00026, 0.00068", "−6.08, −4.32, −3.47, −3.29", "gi|45602121(AAS71599.1)", "Bacterial group 3 Ig-like protein (OmpL47)(LIC_13050)", ""], ["1,610, 1,613", "0.000015, 0.00021", "−6.08, −4.3", "gi|45600128(AAS69614.1)", "Anti-sigma factor antagonist(LIC_11004)", ""], ["1,554", "0.000011", "−5.02", "gi|45601701(AAS71181.1)", "Cell shape determination protein(LIC_12621)", ""], ["1,066, 1,545, 1,529", "0.000023, 0.00096, 0.0059", "−4.81, −2.60, −1.73", "gi|45600754(AAS70238.1)", "Qlp42 = LipL45(LIC_11643)", "FecR protein"], ["637", "3.7E-06", "−4.78", "gi|45600094(AAS69581.1)", "Acyl-CoA dehydrogenase(LIC_10970)", ""], ["580, 581", "6.5E-06, 2.9E-06", "−4.69, −3.83", "gi|45602637(AAS72112.1)", "S-adenosylhomocysteine hydrolase(LIC_20083)", ""], ["1,606", "0.00012", "−4.61", "gi|45601539(AAS71020.1)", "Response regulator(LIC_12454)", ""], ["1,144", "0.000059", "−4.5", "gi|45600133(AAS69619.1)", "Conserved hypothetical protein(LIC_11009)", "None predicted"], ["260, 256", "0.0001, 0.0031", "−4.14, −3.2", "gi|45601779(AAS71259.1)", "Polyribonucleotide nucleotidyltransferase(LIC_12701)", ""], ["333", "0.0015", "−3.53", "gi|45602455(AAS71932.1)", "Polysaccharide deacetylase(LIC_13392)", ""], ["780", "0.00017", "−3.42", "gi|45600315(AAS69801.1)", "Putative citrate lyase(LIC_11194)", ""], ["1,174, 1,177", "0.000066, 0.0047", "−3.13, −1.72", "gi|45600937(AAS70420.1)", "Putative lipoprotein(LIC_11834)", "Fe (2+)-dicitrate sensor, transmembrane component, FecR protein"], ["642", "0.00052", "−3.11", "gi|45602311(AAS71788.1)", "Isocitrate dehydrogenase(LIC_13244)", ""], ["1,495", "0.0071", "−3.07", "gi|45599867(AAS69355.1)", "Conserved hypothetical protein(LIC_10736)", "Endoribonuclease L-PSP/chorismate mutase-like"], ["1,548, 1,556", "0.000052, 0.0029", "−2.93, −2.07", "gi|45601701(AAS71181.1)", "Cell shape determination protein(LIC_12621)", ""], ["1,250", "0.000081", "−2.92", "gi|45600531(AAS70016.1)", "ATP-dependent Clp protease(LIC_11417)", ""], ["432", "0.000084", "−2.67", "gi|45601716(AAS71196.1)", "Rho(LIC_12636)", ""], ["259", "0.00035", "−2.63", "gi|45601070(AAS70553.1)", "Cyclic nucleotide binding protein(LIC_11977)", ""], ["962, 957, 974, 943, 960, 968, 969, 950, 979, 948, 949, 947, 975, 967, 940, 945, 959, 934, 958, 942", "0.00054, 0.0016, 0.0012, 0.00081, 0.00091, 0.0017, 0.0094, 0.0027, 0.0024, 0.0019, 0.0023, 0.0017, 0.041, 0.0044, 0.0023, 0.027, 0.0038, 0.0013, 0.0054, 0.012", "−2.52, −2.51, −2.48, −2.45, −2.33, −2.29, −2.23, −2.21, −2.20, −2.19, −2.17, −2.12, −2.11, −2.1, −2.09, −2.09, −2.07, −2.06, −1.98, −1.92", "gi|45600468(AAS69953.1)", "LipL32(LIC_11352)", ""], ["537, 546", "0.00014, 0.00041", "−2.50, −2.14", "gi|45601560(AAS71041.1)", "Dihydrolipoamide succinyltransferase(LIC_12476)", ""], ["459, 227, 457", "0.012, 0.03, 0.046", "−2.40, −1.69, −1.56", "gi|30652620 (Q72SY1.2)", "ATP synthase subunit alpha(LIC_11241)", ""], ["1,612", "0.00042", "−2.38", "gi|45602544(AAS72021.1)", "Cell shape determination protein(LIC_13483)", ""], ["814", "0.0041", "−2.17", "gi|45600379(AAS69864.1)", "MreB(LIC_11258)", ""], ["254", "0.0022", "−2.13", "gi|45601070(AAS70553.1)", "Cyclic nucleotide binding protein(LIC_11977)", ""], ["725, 717, 701, 711, 710, 706, 704", "0.0068, 0.0035, 0.0067, 0.034, 0.011, 0.0039, 0.05", "−2.07, −1.87, −1.79, −1.67, −1.61, −1.60, −1.45", "gi|45602037(AAS71516.1)", "LipL41(LIC_12966)", "TPR domain"], ["544", "0.014", "−2.06", "gi|45600364(AAS69849.1)", "ATP synthase beta chain(LIC_11243)", ""], ["286", "0.037", "−2.03", "gi|45599657(AAS69145.1)", "DnaK(LIC_10524)", ""], ["1,364, 1,352", "0.02, 0.0081", "−1.78, −1.55", "gi|304570487(AAS69491.1)", "Cytochrome C/hypothetical protein(LIC10877)", ""], ["1,251", "0.028", "−1.71", "gi|45602144(AAS71622.1)", "Transcriptional regulator (TetR family)(LIC_13073)", ""]], "row_count": 35, "column_count": 6, "numeric_cells": 171, "header_rows": 1, "locator": "section[12]/table-wrap[2]#T3"}}], "gaps": ["asset:data:geo:PXD006995 not downloaded", "asset:data:geo:PXD006995 licence not read"]}, "analysis": {"state": "partial", "methods": [{"id": "method-1", "family": "sequence_alignment", "specific": "blast", "label": "Sequence alignment / 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