Metaproteomic assessment of gut microbial and host functional perturbations in Helicobacter pylori-infected patients subjected to an antimicrobial protocol

References

• Dancer SJ. How antibiotics can make us sick: the less obvious adverse effects of antimicrobial chemotherapy. Lancet Infect Dis. 2004;4(10):611–19. doi:10.1016/S1473-3099(04)01145-4.
   PubMed Web of Science ®Google Scholar
• Bhalodi AA, Van Engelen TSR, Virk HS, Wiersinga WJ. Impact of antimicrobial therapy on the gut microbiome. J Antimicrob Chemother. 2019;74(Supplement_1):i6–i15. doi:10.1093/jac/dky530.
   PubMedGoogle Scholar
• Palleja A, Mikkelsen KH, Forslund SK, Kashani A, Allin KH, Nielsen T, Hansen TH, Liang S, Feng Q, Zhang C, et al. Recovery of gut microbiota of healthy adults following antibiotic exposure. Nat Microbiol. 2018;3(11):1255–1265. doi:10.1038/s41564-018-0257-9.
   PubMed Web of Science ®Google Scholar
• Chen J, Siliceo SL, Ni Y, Nielsen HB, Xu A, Panagiotou G. Identification of robust and generalizable biomarkers for microbiome-based stratification in lifestyle interventions. Microbiome. 2023;11(1):178. doi:10.1186/s40168-023-01604-z.
   PubMed Web of Science ®Google Scholar
• Raymond F, Ouameur AA, Déraspe M, Iqbal N, Gingras H, Dridi B, Leprohon P, Plante PL, Giroux R, Bérubé È, et al. The initial state of the human gut microbiome determines its reshaping by antibiotics. ISME J. 2016;10(3):707–720. doi:10.1038/ismej.2015.148.
   PubMed Web of Science ®Google Scholar
• Rashidi A, Ebadi M, Rehman TU, Elhusseini H, Nalluri H, Kaiser T, Holtan SG, Khoruts A, Weisdorf DJ, Staley C. Gut microbiota response to antibiotics is personalized and depends on baseline microbiota. Microbiome. 2021;9(1):211. doi:10.1186/s40168-021-01170-2.
   PubMed Web of Science ®Google Scholar
• Morgun A, Dzutsev A, Dong X, Greer RL, Sexton DJ, Ravel J, Schuster M, Hsiao W, Matzinger P, Shulzhenko N. Uncovering effects of antibiotics on the host and microbiota using transkingdom gene networks. Gut. 2015;64(11):1732–1743. doi:10.1136/gutjnl-2014-308820.
   PubMed Web of Science ®Google Scholar
• Li L, Ning Z, Zhang X, Mayne J, Cheng K, Stintzi A, Figeys D. RapidAIM: a culture- and metaproteomics-based Rapid Assay of Individual Microbiome responses to drugs. Microbiome. 2020;8(1):33. doi:10.1186/s40168-020-00806-z.
   PubMed Web of Science ®Google Scholar
• Dore MP, Sau R, Niolu C, Abbondio M, Tanca A, Bibbò S, Loria M, Pes GM, Uzzau S. Metagenomic changes of gut microbiota following treatment of Helicobacter pylori infection with a Simplified low-Dose quadruple therapy with bismuth or lactobacillus reuteri. Nutrients. 2022;14(14):14. doi:10.3390/nu14142789.
   Web of Science ®Google Scholar
• Metwaly A, Reitmeier S, Haller D. Microbiome risk profiles as biomarkers for inflammatory and metabolic disorders. Nat Rev Gastroenterol Hepatol. 2022;19(6):383–397. doi:10.1038/s41575-022-00581-2.
   PubMed Web of Science ®Google Scholar
• Tang WHW, Kitai T, Hazen SL. Gut microbiota in cardiovascular health and disease. Circ Res. 2017;120(7):1183–1196. doi:10.1161/CIRCRESAHA.117.309715.
   PubMed Web of Science ®Google Scholar
• Budden KF, Gellatly SL, Wood DLA, Cooper MA, Morrison M, Hugenholtz P, Hansbro PM. Emerging pathogenic links between microbiota and the gut–lung axis. Nat Rev Microbiol. 2017;15(1):55–63. doi:10.1038/nrmicro.2016.142.
   PubMed Web of Science ®Google Scholar
• Wu H, Tremaroli V, Bäckhed F. Linking microbiota to human diseases: a systems biology perspective. Trends Endocrinol Metab. 2015;26(12):758–770. doi:10.1016/j.tem.2015.09.011.
   PubMed Web of Science ®Google Scholar
• Kleiner M, Thorson E, Sharp CE, Dong X, Liu D, Li C, Strous M. Assessing species biomass contributions in microbial communities via metaproteomics. Nat Commun. 2017;8(1):1558. doi:10.1038/s41467-017-01544-x.
   PubMed Web of Science ®Google Scholar
• Zhang X, Figeys D. Perspective and Guidelines for Metaproteomics in Microbiome Studies. J Proteome Res. 2019;18(6):2370–2380. doi:10.1021/acs.jproteome.9b00054.
   PubMed Web of Science ®Google Scholar
• Zarrinpar A, Chaix A, Xu ZZ, Chang MW, Marotz CA, Saghatelian A, Knight R, Panda S. Antibiotic-induced microbiome depletion alters metabolic homeostasis by affecting gut signaling and colonic metabolism. Nat Commun. 2018;9(1):2872. doi:10.1038/s41467-018-05336-9.
   PubMed Web of Science ®Google Scholar
• Waite DW, Chuvochina M, Pelikan C, Parks DH, Yilmaz P, Wagner M, Loy A, Naganuma T, Nakai R, Whitman WB, et al. Proposal to reclassify the proteobacterial classes deltaproteobacteria and oligoflexia, and the phylum thermodesulfobacteria into four phyla reflecting major functional capabilities. Int J Syst Evol Microbiol. 2020;70(11):5972–6016. doi:10.1099/ijsem.0.004213.
   PubMed Web of Science ®Google Scholar
• Ohge H, Furne JK, Springfield J, Sueda T, Madoff RD, Levitt MD. The effect of antibiotics and bismuth on fecal hydrogen sulfide and sulfate-reducing bacteria in the rat. FEMS Microbiol Lett. 2003;228(1):137–142. doi:10.1016/S0378-1097(03)00748-1.
   PubMed Web of Science ®Google Scholar
• Palusiak A. Proteus mirabilis and Klebsiella pneumoniae as pathogens capable of causing co-infections and exhibiting similarities in their virulence factors. Front Cell Infect Microbiol. 2022;12:12. doi:10.3389/fcimb.2022.991657.
   Google Scholar
• Chen Q, Wang M, Han M, Xu L, Zhang H. Molecular basis of Klebsiella pneumoniae colonization in host. Microb Pathog. 2023;177:106026. doi:10.1016/j.micpath.2023.106026.
   PubMed Web of Science ®Google Scholar
• Lagkouvardos I, Lesker TR, Hitch TCA, Gálvez EJC, Smit N, Neuhaus K, Wang J, Baines JF, Abt B, Stecher B, et al. Sequence and cultivation study of muribaculaceae reveals novel species, host preference, and functional potential of this yet undescribed family. Microbiome. 2019;7(1):28. doi:10.1186/s40168-019-0637-2.
   PubMed Web of Science ®Google Scholar
• Yang X, Wang Z, Niu J, Zhai R, Xue X, Wu G, Fang Y, Meng G, Yuan H, Zhao L, et al. Pathobionts from chemically disrupted gut microbiota induce insulin-dependent diabetes in mice. Microbiome. 2023;11(1):62. doi:10.1186/s40168-023-01507-z.
   PubMed Web of Science ®Google Scholar
• Joshi S, Shallal A, Zervos M. Vancomycin-Resistant Enterococci: epidemiology, infection Prevention, and control. Infect Dis Clin North Am. 2021;35(4):953–968. doi:10.1016/j.idc.2021.07.002.
   PubMed Web of Science ®Google Scholar
• Ge R, Sun X, Gu Q, Watt RM, Tanner JA, Wong BCY, Xia HH, Huang J-D, He Q-Y, Sun H. A proteomic approach for the identification of bismuth-binding proteins in Helicobacter pylori. JBIC J Biol Inorg Chem. 2007;12(6):831–842. doi:10.1007/s00775-007-0237-7.
   PubMed Web of Science ®Google Scholar
• Hong Y, Lai Y-T, Chan G-F, Sun H. Glutathione and multidrug resistance protein transporter mediate a self-propelled disposal of bismuth in human cells. Proc Natl Acad Sci. 2015;112(11):3211–3216. doi:10.1073/pnas.1421002112.
   PubMed Web of Science ®Google Scholar
• Mikov M. The metabolism of drugs by the gut flora. Eur J Drug Metab Pharmacokinet. 1994;19(3):201–207. doi:10.1007/BF03188922.
   PubMed Web of Science ®Google Scholar
• Cooper AJL, Hanigan MH. 10.17 - Metabolism of Glutathione S-Conjugates: multiple pathways. In: McQueen Charlene A., editor. Comprehensive Toxicology. 3rd ed. Oxford: Elsevier 2018;363–406.
   Google Scholar
• Xu T, Zhou F, Wang L, Wu S, Huang H. Metronidazole-resistant Clostridioides difficile: genomic and transcriptomic traits acquired under in-vitro metronidazole induction. Int J Antimicrob Agents. 2022;59(5):106570. doi:10.1016/j.ijantimicag.2022.106570.
   PubMed Web of Science ®Google Scholar
• Fidelle M, Rauber C, Alves Costa Silva C, Tian A-L, Lahmar I, de La Varende A-L, Zhao L, Thelemaque C, Lebhar I, Messaoudene M, et al. A microbiota-modulated checkpoint directs immunosuppressive intestinal T cells into cancers. Science. 2023;380(6649):eabo2296. doi:10.1126/science.abo2296.
   PubMed Web of Science ®Google Scholar
• Nosova T, Jokelainen K, Kaihovaara P, Jousimies-Somer H, Siitonen A, Heine R, Salaspuro M. Aldehyde dehydrogenase activity and acetate production by aerobic bacteria representing the normal flora of human large intestine. Alcohol Alcohol. 1996;31(6):555–564. doi:10.1093/oxfordjournals.alcalc.a008191.
   PubMed Web of Science ®Google Scholar
• Reichardt N, Duncan SH, Young P, Belenguer A, McWilliam Leitch C, Scott KP, Flint HJ, Louis P. Phylogenetic distribution of three pathways for propionate production within the human gut microbiota. ISME J. 2014;8(6):1323–1335. doi:10.1038/ismej.2014.14.
   PubMed Web of Science ®Google Scholar
• Dimroth P, Hilbi H. Enzymic and genetic basis for bacterial growth on malonate. Mol Microbiol. 1997;25(1):3–10. doi:10.1046/j.1365-2958.1997.4611824.x.
   PubMed Web of Science ®Google Scholar
• Drake HL, Gößner AS, Daniel SL. Old acetogens, new light. Ann N Y Acad Sci. 2008;1125(1):100–128. doi:10.1196/annals.1419.016.
   PubMedGoogle Scholar
• Hosseini E, Grootaert C, Verstraete W, Van de Wiele T. Propionate as a health-promoting microbial metabolite in the human gut. Nutr Rev. 2011;69(5):245–258. doi:10.1111/j.1753-4887.2011.00388.x.
   PubMed Web of Science ®Google Scholar
• Hodgkinson K, El Abbar F, Dobranowski P, Manoogian J, Butcher J, Figeys D, Mack D, Stintzi A. Butyrate’s role in human health and the current progress towards its clinical application to treat gastrointestinal disease. Clin Nutr. 2023;42(2):61–75. doi:10.1016/j.clnu.2022.10.024.
   PubMed Web of Science ®Google Scholar
• Baughn AD, Malamy MH. The strict anaerobe bacteroides fragilis grows in and benefits from nanomolar concentrations of oxygen. Nature. 2004;427(6973):441–444. doi:10.1038/nature02285.
   PubMed Web of Science ®Google Scholar
• Borisov VB, Siletsky SA, Paiardini A, Hoogewijs D, Forte E, Giuffrè A, Poole RK. Bacterial oxidases of the cytochrome bd family: Redox enzymes of unique structure, function, and utility as drug targets. Antioxid Redox Signal. 2021;34(16):1280–1318. doi:10.1089/ars.2020.8039.
   PubMed Web of Science ®Google Scholar
• Butler NL, Ito T, Foreman S, Morgan JE, Zagorevsky D, Malamy MH, Comstock LE, Barquera B, Mullineaux CW. Bacteroides fragilis Maintains Concurrent Capability for Anaerobic and Nanaerobic Respiration. J Bacteriol. 2023;205(1):e00389–22. doi:10.1128/jb.00389-22.
   PubMed Web of Science ®Google Scholar
• Parker BJ, Wearsch PA, Veloo ACM, Rodriguez-Palacios A. The genus alistipes: gut bacteria with emerging implications to inflammation, cancer, and mental health. Front Immunol. 2020;11:11. doi:10.3389/fimmu.2020.00906.
   PubMed Web of Science ®Google Scholar
• White JBR, Silale A, Feasey M, Heunis T, Zhu Y, Zheng H, Gajbhiye A, Firbank S, Baslé A, Trost M, et al. Outer membrane utilisomes mediate glycan uptake in gut Bacteroidetes. Nature. 2023;618(7965):583–589. doi:10.1038/s41586-023-06146-w.
   PubMed Web of Science ®Google Scholar
• Ng KM, Ferreyra JA, Higginbottom SK, Lynch JB, Kashyap PC, Gopinath S, Naidu N, Choudhury B, Weimer BC, Monack DM, et al. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature. 2013;502(7469):96–99. doi:10.1038/nature12503.
   PubMed Web of Science ®Google Scholar
• Stecher B. Finding a sugary foothold: how antibiotics pave the way for enteric pathogens. Cell Host & Microbe. 2013;14(3):225–227. doi:10.1016/j.chom.2013.08.008.
   PubMed Web of Science ®Google Scholar
• Vogt JA, Pencharz PB, Wolever TMS. L-rhamnose increases serum propionate in humans. Am J Clin Nutr. 2004;80(1):89–94. doi:10.1093/ajcn/80.1.89.
   PubMed Web of Science ®Google Scholar
• Kim J, Jin YS, Kim KH. L-Fucose is involved in human–gut microbiome interactions. Appl Microbiol Biotechnol. 2023;107(12):3869–3875. doi:10.1007/s00253-023-12527-y.
   PubMed Web of Science ®Google Scholar
• Hudson AW, Barnes AJ, Bray AS, Ornelles DA, Zafar MA, Raffatellu M. Klebsiella pneumoniae l-Fucose Metabolism Promotes Gastrointestinal Colonization and Modulates Its Virulence Determinants. Infect Immun. 2022;90(10):e00206–22. doi:10.1128/iai.00206-22.
   PubMed Web of Science ®Google Scholar
• Tsai YK, Fung CP, Lin JC, Chen JH, Chang FY, Chen TL, Siu LK. Klebsiella pneumoniae outer membrane porins OmpK35 and OmpK36 play roles in both antimicrobial resistance and virulence. Antimicrob Agents Chemother. 2011;55(4):1485–1493. doi:10.1128/AAC.01275-10.
   PubMed Web of Science ®Google Scholar
• Hellman J, Shaw Warren H. Outer membrane protein a (OmpA), peptidoglycan-associated lipoprotein (PAL), and murein lipoprotein (MLP) are released in experimental Gram-negative sepsis. J Endotoxin Res. 2001;7(1):69–72. doi:10.1177/09680519010070010101.
   PubMedGoogle Scholar
• Wolf PG, Cowley ES, Breister A, Matatov S, Lucio L, Polak P, Ridlon JM, Gaskins HR, Anantharaman K. Diversity and distribution of sulfur metabolic genes in the human gut microbiome and their association with colorectal cancer. Microbiome. 2022;10(1):64. doi:10.1186/s40168-022-01242-x.
   PubMed Web of Science ®Google Scholar
• Cao C, Wang J, Liu Y, Kwok L-Y, Zhang H, Zhang W, Wilmes P. Adaptation of lactobacillus plantarum to ampicillin involves mechanisms that maintain protein homeostasis. mSystems. 2020;5(1):10.1128/msystems.00853–19. doi:10.1128/mSystems.00853-19.
   Web of Science ®Google Scholar
• Illigmann A, Thoma Y, Pan S, Reinhardt L, Brötz-Oesterhelt H. Contribution of the clp protease to bacterial survival and mitochondrial homoeostasis. Microb Physiol. 2021;31(3):260–279. doi:10.1159/000517718.
   PubMedGoogle Scholar
• Agrawal A, Singh PP, Bottazzi B, Garlanda C, Mantovani A. Pattern recognition by pentraxins. In: Kishore U, editor. Advances in experimental medicine and biology. New York, NY: Springer New York; 2009. pp. 98–116.
   Google Scholar
• Lin LL, Chen CN, Lin WC, Lee PH, Chang KJ, Lai YP, Wang JT, Juan HF. Annexin A4: a novel molecular marker for gastric cancer with Helicobacter pylori infection using proteomics approach. Proteomics - Clin Appl. 2008;2(4):619–634. doi:10.1002/prca.200780088.
   PubMed Web of Science ®Google Scholar
• Wang XH, Zhang LH, Zhong XY, Xing XF, Liu YQ, Niu ZJ, Peng Y, Du H, Zhang GG, Hu Y, et al. S100A6 overexpression is associated with poor prognosis and is epigenetically up-regulated in gastric cancer. Am J Pathol. 2010;177(2):586–597. doi:10.2353/ajpath.2010.091217.
   PubMed Web of Science ®Google Scholar
• Montemurro P, Nishioka H, Dundon WG, de Bernard M, Del Giudice G, Rappuoli R, Montecucco C. The neutrophil-activating protein (HP-NAP) of Helicobacter pylori is a potent stimulant of mast cells. Eur J Immunol. 2002;32(3):671–676. doi:10.1002/1521-4141(200203)32:3<671:AID-IMMU671>3.0.CO;2-5.
   PubMed Web of Science ®Google Scholar
• Fukuishi N, Murakami S, Ohno A, Yamanaka N, Matsui N, Fukutsuji K, Yamada S, Itoh K, Akagi M. Does β-hexosaminidase function only as a degranulation indicator in mast cells? The primary role of β-hexosaminidase in mast cell granules. J Immunol. 2014;193(4):1886–1894. doi:10.4049/jimmunol.1302520.
   PubMed Web of Science ®Google Scholar
• Balluff B, Rauser S, Meding S, Elsner M, Schöne C, Feuchtinger A, Schuhmacher C, Novotny A, Jütting U, MacCarrone G, et al. MALDI imaging identifies prognostic seven-protein signature of novel tissue markers in intestinal-type gastric cancer. Am J Pathol. 2011;179(6):2720–2729. doi:10.1016/j.ajpath.2011.08.032.
   PubMed Web of Science ®Google Scholar
• Wang L, Llorente C, Hartmann P, Yang AM, Chen P, Schnabl B. Methods to determine intestinal permeability and bacterial translocation during liver disease. J Immunol Methods. 2015;421:44–53. doi:10.1016/j.jim.2014.12.015.
   PubMed Web of Science ®Google Scholar
• Muñoz L, Borrero MJ, Úbeda M, Conde E, Del Campo R, Rodríguez-Serrano M, Lario M, Sánchez-Díaz AM, Pastor O, Díaz D, et al. Intestinal immune dysregulation driven by dysbiosis promotes barrier disruption and bacterial translocation in rats with cirrhosis. Hepatology. 2019;70(3):925–938. doi:10.1002/hep.30349.
   PubMed Web of Science ®Google Scholar
• Li S, Mao Q, Zhang Z, Wang Y, Chen D, Chen Z, Lu J. Identification of a Five-gene Panel to assess prognosis for gastric cancer. Biomed Res Int. 2022;2022:1–9. doi:10.1155/2022/5593619.
   Web of Science ®Google Scholar
• Nagata N, Akiyama J, Marusawa H, Shimbo T, Liu Y, Igari T, Nakashima R, Watanabe H, Uemura N, Chiba T. Enhanced expression of activation-induced cytidine deaminase in human gastric mucosa infected by Helicobacter pylori and its decrease following eradication. J Gastroenterol. 2014;49(3):427–435. doi:10.1007/s00535-013-0808-z.
   PubMed Web of Science ®Google Scholar
• Matsumoto Y, Marusawa H, Kinoshita K, Endo Y, Kou T, Morisawa T, Azuma T, Okazaki IM, Honjo T, Chiba T. Helicobacter pylori infection triggers aberrant expression of activation-induced cytidine deaminase in gastric epithelium. Nat Med. 2007;13(4):470–476. doi:10.1038/nm1566.
   PubMed Web of Science ®Google Scholar
• Lu C, Amin MA, Fox DA. CD13/Aminopeptidase N is a potential therapeutic target for inflammatory disorders. J Immunol. 2020;204(1):3–11. doi:10.4049/jimmunol.1900868.
   PubMed Web of Science ®Google Scholar
• Garay J, Piazuelo MB, Lopez-Carrillo L, Leal YA, Majumdar S, Li L, Cruz-Rodriguez N, Serrano-Gomez SJ, Busso CS, Schneider BG, et al. Increased expression of deleted in malignant brain tumors (DMBT1) gene in precancerous gastric lesions: findings from human and animal studies. Oncotarget. 2017;8(29):47076–47089. doi:10.18632/oncotarget.16792.
   PubMedGoogle Scholar
• Madsen J, Mollenhauer J, Holmskov U. Review: Gp-340/DMBT1 in mucosal innate immunity. Innate Immun. 2010;16(3):160–167. doi:10.1177/1753425910368447.
   PubMed Web of Science ®Google Scholar
• Park HS, Kim BC, Yeo HY, Kim KH, Yoo BC, Park JW, Chang HJ. Deleted in malignant brain tumor 1 is a novel prognostic marker in colorectal cancer. Oncol Rep. 2018;39:2279–2287. doi:10.3892/or.2018.6287.
   PubMed Web of Science ®Google Scholar
• Mondola P, Damiano S, Sasso A, Santillo M. The Cu, Zn superoxide dismutase: not only a dismutase enzyme. Front Physiol. 2016;7:7. doi:10.3389/fphys.2016.00594.
   PubMed Web of Science ®Google Scholar
• Tanca A, Palomba A, Pisanu S, Deligios M, Fraumene C, Manghina V, Pagnozzi D, Addis MF, Uzzau S. A straightforward and efficient analytical pipeline for metaproteome characterization. Microbiome. 2014;2(1):49. doi:10.1186/s40168-014-0049-2.
   PubMed Web of Science ®Google Scholar
• Wiśniewski JR, Zougman A, Nagaraj N, Mann M. Universal sample preparation method for proteome analysis. Nat Methods. 2009;6(5):359–362. doi:10.1038/nmeth.1322.
   PubMed Web of Science ®Google Scholar
• Tanca A, Biosa G, Pagnozzi D, Addis MF, Uzzau S. Comparison of detergent-based sample preparation workflows for LTQ-Orbitrap analysis of the Escherichia coli proteome. Proteomics. 2013;13(17):2597–2607. doi:10.1002/pmic.201200478.
   PubMed Web of Science ®Google Scholar
• Taverna D, Gaspari M. A critical comparison of three MS-based approaches for quantitative proteomics analysis. J Mass Spectrom. 2021;56(1):e4669. doi:10.1002/jms.4669.
   PubMed Web of Science ®Google Scholar
• Li J, Jia H, Cai X, Zhong H, Feng Q, Sunagawa S, Arumugam M, Kultima JR, Prifti E, Nielsen T, et al. An integrated catalog of reference genes in the human gut microbiome. Nat Biotechnol. 2014;32(8):834–841. doi:10.1038/nbt.2942.
   PubMed Web of Science ®Google Scholar
• Verschaffelt P, Van Den Bossche T, Martens L, Dawyndt P, Mesuere B. Unipept desktop: a faster, more powerful metaproteomics results analysis tool. J Proteome Res. 2021;20(4):2005–2009. doi:10.1021/acs.jproteome.0c00855.
   PubMed Web of Science ®Google Scholar
• Cantalapiedra CP, Hern̗andez-Plaza A, Letunic I, Bork P, Huerta-Cepas J. eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol. 2021;38(12):5825–5829. doi:10.1093/molbev/msab293.
   PubMed Web of Science ®Google Scholar
• Kanehisa M, Furumichi M, Sato Y, Kawashima M, Ishiguro-Watanabe M. KEGG for taxonomy-based analysis of pathways and genomes. Nucleic Acids Res. 2023;51(D1):D587–92. doi:10.1093/nar/gkac963.
   PubMed Web of Science ®Google Scholar
• Porcheddu M, Abbondio M, De Diego L, Uzzau S, Tanca A. Meta4P: a user-friendly tool to parse label-free quantitative metaproteomic data and taxonomic/functional annotations. J Proteome Res. 2023;22(6):2109–2113. doi:10.1021/acs.jproteome.2c00803.
   PubMed Web of Science ®Google Scholar
• Metsalu T, Vilo J. ClustVis: a web tool for visualizing clustering of multivariate data using Principal component analysis and heatmap. Nucleic Acids Res. 2015;43(W1):W566–70. doi:10.1093/nar/gkv468.
   PubMed Web of Science ®Google Scholar
• Tyanova S, Temu T, Sinitcyn P, Carlson A, Hein MY, Geiger T, Mann M, Cox J. The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat Methods. 2016;13(9):731–740. doi:10.1038/nmeth.3901.
   PubMed Web of Science ®Google Scholar
• Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B. 1995;57(1):289–300. doi:10.1111/j.2517-6161.1995.tb02031.x.
   Google Scholar
• Perez-Riverol Y, Bai J, Bandla C, García-Seisdedos D, Hewapathirana S, Kamatchinathan S, Kundu DJ, Prakash A, Frericks-Zipper A, Eisenacher M, et al. The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences. Nucleic Acids Res. 2022;50(D1):D543–52. doi:10.1093/nar/gkab1038.
   PubMed Web of Science ®Google Scholar