Reconstruction and modeling protein translocation and compartmentalization in Escherichia coli at the genome-scale

Liu, Joanne K.; O’Brien, Edward J.; Lerman, Joshua A.; Zengler, Karsten; Palsson, Bernhard O.; Feist, Adam M.

doi:10.1186/s12918-014-0110-6

Reconstruction and modeling protein translocation and compartmentalization in Escherichia coli at the genome-scale

Journal Article · Thu Sep 18 00:00:00 EDT 2014 · BMC Systems Biology

DOI:https://doi.org/10.1186/s12918-014-0110-6· OSTI ID:1626877

Liu, Joanne K. ^[1]; O’Brien, Edward J. ^[2]; Lerman, Joshua A. ^[2]; Zengler, Karsten ^[3]; Palsson, Bernhard O. ^[4]; Feist, Adam M. ^[3]

Univ. of California, San Diego, CA (United States). Bioinformatics and Systems Biology; DOE/OSTI
Univ. of California, San Diego, CA (United States). Bioinformatics and Systems Biology
Univ. of California, San Diego, CA (United States). Dept. of Bioengineering; Technical Univ. of Denmark, Lyngby (Denmark). Novo Nordisk Foundation Center for Biosustainability
Univ. of California, San Diego, CA (United States). Bioinformatics and Systems Biology; Univ. of California, San Diego, CA (United States). Dept. of Bioengineering; Univ. of California, San Diego, CA (United States). Dept. of Pediatrics; Technical Univ. of Denmark, Lyngby (Denmark). Novo Nordisk Foundation Center for Biosustainability

Background: Membranes play a crucial role in cellular functions. Membranes provide a physical barrier, control the trafficking of substances entering and leaving the cell, and are a major determinant of cellular ultra-structure. In addition, components embedded within the membrane participate in cell signaling, energy transduction, and other critical cellular functions. All these processes must share the limited space in the membrane; thus it represents a notable constraint on cellular functions. Membrane- and location-based processes have not yet been reconstructed and explicitly integrated into genome-scale models. Results: The recent genome-scale model of metabolism and protein expression in Escherichia coli (called a ME-model) computes the complete composition of the proteome required to perform whole cell functions. Here we expand the ME-model to include (1) a reconstruction of protein translocation pathways, (2) assignment of all cellular proteins to one of four compartments (cytoplasm, inner membrane, periplasm, and outer membrane) and a translocation pathway, (3) experimentally determined translocase catalytic and porin diffusion rates, and (4) a novel membrane constraint that reflects cell morphology. Comparison of computations performed with this expanded ME-model, named iJL1678-ME, against available experimental data reveals that the model accurately describes translocation pathway expression and the functional proteome by compartmentalized mass. Conclusion: iJL1678-ME enables the computation of cellular phenotypes through an integrated computation of proteome composition, abundance, and activity in four cellular compartments (cytoplasm, periplasm, inner and outer membrane). Reconstruction and validation of the model has demonstrated that the iJL1678-ME is capable of capturing the functional content of membranes, cellular compartment-specific composition, and that it can be utilized to examine the effect of perturbing an expanded set of network components. iJL1678-ME takes a notable step towards the inclusion of cellular ultra-structure in genome-scale models.

View Accepted Manuscript (DOE)

Research Organization:: Stanford Univ., CA (United States); Univ. of California, San Diego, CA (United States)

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

Grant/Contract Number:: SC0002009; SC0004917

OSTI ID:: 1626877

Journal Information:: BMC Systems Biology, Journal Name: BMC Systems Biology Journal Issue: 1 Vol. 8; ISSN 1752-0509

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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Improving the phenotype predictions of a yeast genome‐scale metabolic model by incorporating enzymatic constraints Sánchez, Benjamín J.; Zhang, Cheng; Nilsson, Avlant Molecular Systems Biology, Vol. 13, Issue 8 https://doi.org/10.15252/msb.20167411	journal	August 2017
Lean-Proteome Strains â€“ Next Step in Metabolic Engineering Valgepea, Kaspar; Peebo, Karl; Adamberg, Kaarel Frontiers in Bioengineering and Biotechnology, Vol. 3 https://doi.org/10.3389/fbioe.2015.00011	journal	February 2015
Analysis of genetic variation and potential applications in genome-scale metabolic modeling Cardoso, João Frontiers in Bioengineering and Biotechnology, Vol. 3 https://doi.org/10.3389/fbioe.2015.00013	journal	January 2015
A system-wide network reconstruction of gene regulation and metabolism in Escherichia coli Grimbs, Anne; Klosik, David F.; Bornholdt, Stefan arXiv https://doi.org/10.48550/arxiv.1803.05429	text	January 2018
Additional file 1 of Adaptations of Escherichia coli strains to oxidative stress are reflected in properties of their structural proteomes Mih, Nathan; Monk, Jonathan M.; Fang, Xin figshare https://doi.org/10.6084/m9.figshare.12218915.v1	dataset	January 2020
Optimizing eukaryotic cell hosts for protein production through systems biotechnology and genome-scale modeling Gutierrez, Jahir M.; Lewis, Nathan E. Biotechnology Journal, Vol. 10, Issue 7 https://doi.org/10.1002/biot.201400647	journal	June 2015
Genome-scale metabolic models applied to human health and disease: Genome-scale metabolic models Cook, Daniel J.; Nielsen, Jens Wiley Interdisciplinary Reviews: Systems Biology and Medicine, Vol. 9, Issue 6 https://doi.org/10.1002/wsbm.1393	journal	June 2017
Channel crossing: how are proteins shipped across the bacterial plasma membrane? Collinson, Ian; Corey, Robin A.; Allen, William J. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 370, Issue 1679 https://doi.org/10.1098/rstb.2015.0025	journal	October 2015
Enzymes and Substrates Are Balanced at Minimal Combined Mass Concentration in vivo Dourado, Hugo; Maurino, Veronica G.; Lercher, Martin J. bioRxiv https://doi.org/10.1101/128009	posted_content	April 2017
The y-ome defines the thirty-four percent of Escherichia coli genes that lack experimental evidence of function Ghatak, Sankha; King, Zachary A.; Sastry, Anand bioRxiv https://doi.org/10.1101/328591	posted_content	December 2018
Genome-scale reconstructions of the mammalian secretory pathway predict metabolic costs and limitations of protein secretion Gutierrez, Jahir M.; Feizi, Amir; Li, Shangzhong bioRxiv https://doi.org/10.1101/351387	posted_content	November 2019
Modelling the metabolism of protein secretion through the Tat route in Streptomyces lividans Valverde, José R.; Gullón, Sonia; Mellado, Rafael P. BMC Microbiology, Vol. 18, Issue 1 https://doi.org/10.1186/s12866-018-1199-3	journal	June 2018
COBRAme: A computational framework for genome-scale models of metabolism and gene expression Lloyd, Colton J.; Ebrahim, Ali; Yang, Laurence PLOS Computational Biology, Vol. 14, Issue 7 https://doi.org/10.1371/journal.pcbi.1006302	journal	July 2018
A system-wide network reconstruction of gene regulation and metabolism in Escherichia coli Grimbs, Anne; Klosik, David F.; Bornholdt, Stefan PLOS Computational Biology, Vol. 15, Issue 5 https://doi.org/10.1371/journal.pcbi.1006962	journal	May 2019
Genome-scale model of metabolism and gene expression provides a multi-scale description of acid stress responses in Escherichia coli Du, Bin; Yang, Laurence; Lloyd, Colton J. PLOS Computational Biology, Vol. 15, Issue 12 https://doi.org/10.1371/journal.pcbi.1007525	journal	December 2019

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59 BASIC BIOLOGICAL SCIENCES
Constraint-based modeling
Mathematical & Computational Biology
compartmentalization
gene expression
metabolism
protein translocation

Reconstruction and modeling protein translocation and compartmentalization in Escherichia coli at the genome-scale

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