Multi-Omics integration can be used to rescue metabolic information for some of the dark region of the Pseudomonas putida proteome

Tavis, Steven; Hettich, Robert L.

doi:10.1186/s12864-024-10082-y

Title: Multi-Omics integration can be used to rescue metabolic information for some of the dark region of the Pseudomonas putida proteome

Journal Article · 11 March 2024 · BMC Genomics

DOI: https://doi.org/10.1186/s12864-024-10082-y · OSTI ID:2351080

Tavis, Steven ^[1]; Hettich, Robert L. ^[2]

Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

In every omics experiment, genes or their products are identified for which even state of the art tools are unable to assign a function. In the biotechnology chassis organism Pseudomonas putida, these proteins of unknown function make up 14% of the proteome. This missing information can bias analyses since these proteins can carry out functions which impact the engineering of organisms. As a consequence of predicting protein function across all organisms, function prediction tools generally fail to use all of the types of data available for any specific organism, including protein and transcript expression information. Additionally, the release of Alphafold predictions for all Uniprot proteins provides a novel opportunity for leveraging structural information. We constructed a bespoke machine learning model to predict the function of recalcitrant proteins of unknown function in Pseudomonas putida based on these sources of data, which annotated 1079 terms to 213 proteins. Among the predicted functions supplied by the model, we found evidence for a significant overrepresentation of nitrogen metabolism and macromolecule processing proteins. These findings were corroborated by manual analyses of selected proteins which identified, among others, a functionally unannotated operon that likely encodes a branch of the shikimate pathway.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 2351080

Journal Information:: BMC Genomics, Journal Name: BMC Genomics Journal Issue: 1 Vol. 25; ISSN 1471-2164

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

References (54)

Scoring function for automated assessment of protein structure template quality Zhang, Yang; Skolnick, Jeffrey Proteins: Structure, Function, and Bioinformatics, Vol. 57, Issue 4 https://doi.org/10.1002/prot.20264	journal	January 2004
Structure is three to ten times more conserved than sequence-A study of structural response in protein cores Illergård, Kristoffer; Ardell, David H.; Elofsson, Arne Proteins: Structure, Function, and Bioinformatics, Vol. 77, Issue 3 https://doi.org/10.1002/prot.22458	journal	November 2009
Assessment of template based protein structure predictions in CASP9 Mariani, Valerio; Kiefer, Florian; Schmidt, Tobias Proteins: Structure, Function, and Bioinformatics, Vol. 79, Issue S10 https://doi.org/10.1002/prot.23177	journal	January 2011
Depicting a protein's two faces: GPCR classification by phylogenetic tree‐based HMMs Qian, Bin; Soyer, Orkun S.; Neubig, Richard R. FEBS Letters, Vol. 554, Issue 1-2 https://doi.org/10.1016/S0014-5793(03)01112-8	journal	October 2003
Lignin valorization by bacterial genus Pseudomonas: State-of-the-art review and prospects Kumar, Manish; You, Siming; Beiyuan, Jingzi Bioresource Technology, Vol. 320 https://doi.org/10.1016/j.biortech.2020.124412	journal	January 2021
Eliminating a global regulator of carbon catabolite repression enhances the conversion of aromatic lignin monomers to muconate in Pseudomonas putida KT2440 Johnson, Christopher W.; Abraham, Paul E.; Linger, Jeffrey G. Metabolic Engineering Communications, Vol. 5 https://doi.org/10.1016/j.meteno.2017.05.002	journal	December 2017
Pseudomonas putida as a functional chassis for industrial biocatalysis: From native biochemistry to trans-metabolism Nikel, Pablo I.; de Lorenzo, Víctor Metabolic Engineering, Vol. 50 https://doi.org/10.1016/j.ymben.2018.05.005	journal	November 2018
Improving Proteomics Data Reproducibility with a Dual-Search Strategy Fernández-Costa, Carolina; Martínez-Bartolomé, Salvador; McClatchy, Daniel Analytical Chemistry, Vol. 92, Issue 2 https://doi.org/10.1021/acs.analchem.9b04955	journal	December 2019
Ultrafast Peptide Label-Free Quantification with FlashLFQ Millikin, Robert J.; Solntsev, Stefan K.; Shortreed, Michael R. Journal of Proteome Research, Vol. 17, Issue 1 https://doi.org/10.1021/acs.jproteome.7b00608	journal	November 2017
Extremely Fast and Accurate Open Modification Spectral Library Searching of High-Resolution Mass Spectra Using Feature Hashing and Graphics Processing Units Bittremieux, Wout; Laukens, Kris; Noble, William Stafford Journal of Proteome Research, Vol. 18, Issue 10 https://doi.org/10.1021/acs.jproteome.9b00291	journal	August 2019
Gene Ontology: tool for the unification of biology Ashburner, Michael; Ball, Catherine A.; Blake, Judith A. Nature Genetics, Vol. 25, Issue 1 https://doi.org/10.1038/75556	journal	May 2000
A large-scale evaluation of computational protein function prediction Radivojac, Predrag; Clark, Wyatt T.; Oron, Tal Ronnen Nature Methods, Vol. 10, Issue 3 https://doi.org/10.1038/nmeth.2340	journal	January 2013
Fast and sensitive protein alignment using DIAMOND Buchfink, Benjamin; Xie, Chao; Huson, Daniel H. Nature Methods, Vol. 12, Issue 1 https://doi.org/10.1038/nmeth.3176	journal	November 2014
Announcing the worldwide Protein Data Bank Berman, Helen; Henrick, Kim; Nakamura, Haruki Nature Structural & Molecular Biology, Vol. 10, Issue 12 https://doi.org/10.1038/nsb1203-980	journal	December 2003
Environmental conditions shape the nature of a minimal bacterial genome Antczak, Magdalena; Michaelis, Martin; Wass, Mark N. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-10837-2	journal	July 2019
Array programming with NumPy Harris, Charles R.; Millman, K. Jarrod; van der Walt, Stéfan J. Nature, Vol. 585, Issue 7825 https://doi.org/10.1038/s41586-020-2649-2	journal	September 2020
Highly accurate protein structure prediction with AlphaFold Jumper, John; Evans, Richard; Pritzel, Alexander Nature https://doi.org/10.1038/s41586-021-03819-2	journal	July 2021
SignalP 5.0 improves signal peptide predictions using deep neural networks Almagro Armenteros, José Juan; Tsirigos, Konstantinos D.; Sønderby, Casper Kaae Nature Biotechnology, Vol. 37, Issue 4 https://doi.org/10.1038/s41587-019-0036-z	journal	February 2019
Philosopher: a versatile toolkit for shotgun proteomics data analysis da Veiga Leprevost, Felipe; Haynes, Sarah E.; Avtonomov, Dmitry M. Nature Methods, Vol. 17, Issue 9 https://doi.org/10.1038/s41592-020-0912-y	journal	July 2020
Bioprocess development for muconic acid production from aromatic compounds and lignin Salvachúa, Davinia; Johnson, Christopher W.; Singer, Christine A. Green Chemistry, Vol. 20, Issue 21 https://doi.org/10.1039/C8GC02519C	journal	January 2018
The shikimate pathway: gateway to metabolic diversity Shende, Vikram V.; Bauman, Katherine D.; Moore, Bradley S. Natural Product Reports, Vol. 41, Issue 4 https://doi.org/10.1039/D3NP00037K	journal	January 2024
Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles Subramanian, A.; Tamayo, P.; Mootha, V. K. Proceedings of the National Academy of Sciences, Vol. 102, Issue 43, p. 15545-15550 https://doi.org/10.1073/pnas.0506580102	journal	September 2005
Lignin valorization through integrated biological funneling and chemical catalysis Linger, J. G.; Vardon, D. R.; Guarnieri, M. T. Proceedings of the National Academy of Sciences, Vol. 111, Issue 33, p. 12013-12018 https://doi.org/10.1073/pnas.1410657111	journal	August 2014
Proteome Profiling Outperforms Transcriptome Profiling for Coexpression Based Gene Function Prediction Wang, Jing; Ma, Zihao; Carr, Steven A. Molecular & Cellular Proteomics, Vol. 16, Issue 1 https://doi.org/10.1074/mcp.M116.060301	journal	November 2016
The BioCyc collection of microbial genomes and metabolic pathways Karp, Peter D.; Billington, Richard; Caspi, Ron Briefings in Bioinformatics, Vol. 20, Issue 4 https://doi.org/10.1093/bib/bbx085	journal	August 2017
ProteoWizard: open source software for rapid proteomics tools development Kessner, Darren; Chambers, Matt; Burke, Robert Bioinformatics, Vol. 24, Issue 21 https://doi.org/10.1093/bioinformatics/btn323	journal	July 2008
lDDT: a local superposition-free score for comparing protein structures and models using distance difference tests Mariani, Valerio; Biasini, Marco; Barbato, Alessandro Bioinformatics, Vol. 29, Issue 21 https://doi.org/10.1093/bioinformatics/btt473	journal	August 2013
RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference Kozlov, Alexey M.; Darriba, Diego; Flouri, Tomáš Bioinformatics, Vol. 35, Issue 21 https://doi.org/10.1093/bioinformatics/btz305	journal	May 2019
The Gene Ontology knowledgebase in 2023 GENETICS, Vol. 224, Issue 1 https://doi.org/10.1093/genetics/iyad031	journal	March 2023
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
The Protein Data Bank Berman, H. M. Nucleic Acids Research, Vol. 28, Issue 1 https://doi.org/10.1093/nar/28.1.235	journal	January 2000
AlphaFold Protein Structure Database: massively expanding the structural coverage of protein-sequence space with high-accuracy models Varadi, Mihaly; Anyango, Stephen; Deshpande, Mandar Nucleic Acids Research, Vol. 50, Issue D1 https://doi.org/10.1093/nar/gkab1061	journal	November 2021
NetGO 2.0: improving large-scale protein function prediction with massive sequence, text, domain, family and network information Yao, Shuwei; You, Ronghui; Wang, Shaojun Nucleic Acids Research, Vol. 49, Issue W1 https://doi.org/10.1093/nar/gkab398	journal	May 2021
UniProt: the Universal Protein Knowledgebase in 2023 Nucleic Acids Research, Vol. 51, Issue D1 https://doi.org/10.1093/nar/gkac1052	journal	November 2022
The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes Ruepp, A. Nucleic Acids Research, Vol. 32, Issue 18 https://doi.org/10.1093/nar/gkh894	journal	October 2004
TM-align: a protein structure alignment algorithm based on the TM-score Zhang, Y. Nucleic Acids Research, Vol. 33, Issue 7 https://doi.org/10.1093/nar/gki524	journal	April 2005
Enhanced annotations and features for comparing thousands of Pseudomonas genomes in the Pseudomonas genome database Winsor, Geoffrey L.; Griffiths, Emma J.; Lo, Raymond Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1227	journal	November 2015
STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets Szklarczyk, Damian; Gable, Annika L.; Lyon, David Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky1131	journal	November 2018
NetGO: improving large-scale protein function prediction with massive network information You, Ronghui; Yao, Shuwei; Xiong, Yi Nucleic Acids Research, Vol. 47, Issue W1 https://doi.org/10.1093/nar/gkz388	journal	May 2019
An assessment of genome annotation coverage across the bacterial tree of life Lobb, Briallen; Tremblay, Benjamin Jean-Marie; Moreno-Hagelsieb, Gabriel Microbial Genomics, Vol. 6, Issue 3 https://doi.org/10.1099/mgen.0.000341	journal	March 2020
Predicting Protein Function by Genomic Context: Quantitative Evaluation and Qualitative Inferences Huynen, M. Genome Research, Vol. 10, Issue 8 https://doi.org/10.1101/gr.10.8.1204	journal	August 2000
Equivalence between modularity optimization and maximum likelihood methods for community detection Newman, M. E. J. Physical Review E, Vol. 94, Issue 5 https://doi.org/10.1103/PhysRevE.94.052315	journal	November 2016
Fifty-five years of enzyme classification: advances and difficulties McDonald, Andrew G.; Tipton, Keith F. FEBS Journal, Vol. 281, Issue 2 https://doi.org/10.1111/febs.12530	journal	October 2013
Proteinortho: Detection of (Co-)orthologs in large-scale analysis Lechner, Marcus; Findeiß, Sven; Steiner, Lydia BMC Bioinformatics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2105-12-124	journal	April 2011
Homology-based inference sets the bar high for protein function prediction Hamp, Tobias; Kassner, Rebecca; Seemayer, Stefan BMC Bioinformatics, Vol. 14, Issue S3 https://doi.org/10.1186/1471-2105-14-S3-S7	journal	February 2013
Comprehensive analysis of pseudogenes in prokaryotes: widespread gene decay and failure of putative horizontally transferred genes Liu, Yang; Harrison, Paul M.; Kunin, Victor Genome Biology, Vol. 5, Issue 9, p. R64 https://doi.org/10.1186/gb-2004-5-9-r64	journal	January 2004
The CAFA challenge reports improved protein function prediction and new functional annotations for hundreds of genes through experimental screens Zhou, Naihui; Jiang, Yuxiang; Bergquist, Timothy R. Genome Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s13059-019-1835-8	journal	November 2019
The Extinction Dynamics of Bacterial Pseudogenes Kuo, Chih-Horng; Ochman, Howard PLoS Genetics, Vol. 6, Issue 8 https://doi.org/10.1371/journal.pgen.1001050	journal	August 2010
RUPEE: A fast and accurate purely geometric protein structure search Ayoub, Ronald; Lee, Yugyung PLOS ONE, Vol. 14, Issue 3 https://doi.org/10.1371/journal.pone.0213712	journal	March 2019
Stan : A Probabilistic Programming Language Carpenter, Bob; Gelman, Andrew; Hoffman, Matthew D. Journal of Statistical Software, Vol. 76, Issue 1 https://doi.org/10.18637/jss.v076.i01	journal	January 2017
Exploring Network Structure, Dynamics, and Function using NetworkX Hagberg, Aric A.; Schult, Daniel A.; Swart, Pieter J. Proceedings of the Python in Science Conference https://doi.org/10.25080/TCWV9851	conference	June 2008
Finding New Cell Wall Regulatory Genes in Populus trichocarpa Using Multiple Lines of Evidence Furches, Anna; Kainer, David; Weighill, Deborah Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.01249	journal	October 2019
ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees Zhang, Chao; Rabiee, Maryam; Sayyari, Erfan figshare https://doi.org/10.6084/m9.figshare.c.4093409.v1	collection	January 2018
The CAFA challenge reports improved protein function prediction and new functional annotations for hundreds of genes through experimental screens Zhou, Naihui; Jiang, Yuxiang; Bergquist, Timothy figshare https://doi.org/10.6084/m9.figshare.c.4745834.v1	collection	January 2019

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60 APPLIED LIFE SCIENCES
Function prediction
Gene ontology
Machine learning
Multi-omics integration
Proteins of unknown function
Pseudomonas putida

Title: Multi-Omics integration can be used to rescue metabolic information for some of the dark region of the Pseudomonas putida proteome

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