Metabolomics Analysis of Bacterial Pathogen Burkholderia thailandensis and Mammalian Host Cells in Co-culture

Aiosa, Nicole; Sinha, Anupama; Jaiyesimi, Olakunle A.; da Silva, Ricardo R.; Branda, Steven S.; Garg, Neha

doi:10.1021/acsinfecdis.2c00233

Metabolomics Analysis of Bacterial Pathogen Burkholderia thailandensis and Mammalian Host Cells in Co-culture

Journal Article · Wed Jun 29 00:00:00 EDT 2022 · ACS Infectious Diseases

DOI:https://doi.org/10.1021/acsinfecdis.2c00233· OSTI ID:1877157

Aiosa, Nicole ^[1]; Sinha, Anupama ^[2]; Jaiyesimi, Olakunle A. ^[1]; da Silva, Ricardo R. ^[3]; Branda, Steven S. ^[2]; ^[1]

Georgia Institute of Technology, Atlanta, GA (United States)
Sandia National Lab. (SNL-CA), Livermore, CA (United States)
Univ. of Sao Paulo (Brazil)

The Tier 1 HHS/USDA Select Agent Burkholderia pseudomallei is a bacterial pathogen that is highly virulent when introduced into the respiratory tract and intrinsically resistant to many antibiotics. Transcriptomic- and proteomic-based methodologies have been used to investigate mechanisms of virulence employed by B. pseudomallei and Burkholderia thailandensis, a convenient surrogate; however, analysis of the pathogen and host metabolomes during infection is lacking. Changes in the metabolites produced can be a result of altered gene expression and/or post-transcriptional processes. Thus, metabolomics complements transcriptomics and proteomics by providing a chemical readout of a biological phenotype, which serves as a snapshot of an organism’s physiological state. However, the poor signal from bacterial metabolites in the context of infection poses a challenge in their detection and robust annotation. In this work, we coupled mammalian cell culture-based metabolomics with feature-based molecular networking of mono- and co-cultures to annotate the pathogen’s secondary metabolome during infection of mammalian cells. These methods enabled us to identify several key secondary metabolites produced by B. thailandensis during infection of airway epithelial and macrophage cell lines. Additionally, the use of in silico approaches provided insights into shifts in host biochemical pathways relevant to defense against infection. Using chemical class enrichment analysis, for example, we identified changes in a number of host-derived compounds including immune lipids such as prostaglandins, which were detected exclusively upon pathogen challenge. Taken together, our findings indicate that co-culture of B. thailandensis with mammalian cells alters the metabolome of both pathogen and host and provides a new dimension of information for in-depth analysis of the host–pathogen interactions underlying Burkholderia infection.

View Accepted Manuscript (DOE)

Research Organization:: Sandia National Laboratories (SNL-CA), Livermore, CA (United States); Sandia National Laboratories (SNL-NM), Albuquerque, NM (United States)

Sponsoring Organization:: USDOE Laboratory Directed Research and Development (LDRD) Program; USDOE National Nuclear Security Administration (NNSA)

Grant/Contract Number:: AC04-94AL85000; NA0003525

OSTI ID:: 1877157

Report Number(s):: SAND2022-9159J; 708026

Journal Information:: ACS Infectious Diseases, Journal Name: ACS Infectious Diseases Journal Issue: 8 Vol. 8; ISSN 2373-8227

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

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The Condition-Dependent Transcriptional Landscape of Burkholderia pseudomallei Ooi, Wen Fong; Ong, Catherine; Nandi, Tannistha PLoS Genetics, Vol. 9, Issue 9 https://doi.org/10.1371/journal.pgen.1003795	journal	September 2013
Post-Exposure Therapeutic Efficacy of COX-2 Inhibition against Burkholderia pseudomallei Asakrah, Saja; Nieves, Wildaliz; Mahdi, Zaid PLoS Neglected Tropical Diseases, Vol. 7, Issue 5 https://doi.org/10.1371/journal.pntd.0002212	journal	May 2013
Reduced levels of N’-methyl-2-pyridone-5-carboxamide and lysophosphatidylcholine 16:0 in the serum of patients with intrahepatic cholangiocarcinoma, and the correlation with recurrence-free survival Kim, Kyung-Hee; Joo, Jungnam; Park, Boram Oncotarget, Vol. 8, Issue 68 https://doi.org/10.18632/oncotarget.22607	journal	November 2017
A Simple, Reproducible, Inexpensive, Yet Old-Fashioned Method for Determining Phagocytic and Bactericidal Activities of Macrophages Kaneko, Masakazu; Emoto, Yoshiko; Emoto, Masashi Yonsei Medical Journal, Vol. 57, Issue 2 https://doi.org/10.3349/ymj.2016.57.2.283	journal	January 2016
Burkholderia mallei and Burkholderia pseudomallei stimulate differential inflammatory responses from human alveolar type II cells (ATII) and macrophages Lu, Richard; Popov, Vsevolod; Patel, Jignesh Frontiers in Cellular and Infection Microbiology, Vol. 2 https://doi.org/10.3389/fcimb.2012.00165	journal	January 2012
Mechanisms of Disease: Host-Pathogen Interactions between Burkholderia Species and Lung Epithelial Cells David, Jonathan; Bell, Rachel E.; Clark, Graeme C. Frontiers in Cellular and Infection Microbiology, Vol. 5 https://doi.org/10.3389/fcimb.2015.00080	journal	November 2015
Type III Secretion in the Melioidosis Pathogen Burkholderia pseudomallei Vander Broek, Charles W.; Stevens, Joanne M. Frontiers in Cellular and Infection Microbiology, Vol. 7 https://doi.org/10.3389/fcimb.2017.00255	journal	June 2017
Proteomic Profiling of Burkholderia thailandensis During Host Infection Using Bio-Orthogonal Noncanonical Amino Acid Tagging (BONCAT) Franco, Magdalena; D'haeseleer, Patrik M.; Branda, Steven S. Frontiers in Cellular and Infection Microbiology, Vol. 8 https://doi.org/10.3389/fcimb.2018.00370	journal	October 2018
The Burkholderia Type VI Secretion System 5: Composition, Regulation and Role in Virulence Lennings, Jan; West, T. Eoin; Schwarz, Sandra Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.03339	journal	January 2019
Functions of Sphingolipids in Pathogenesis During Host–Pathogen Interactions Wang, Jian; Chen, Yi-Li; Li, Yong-Kang Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.701041	journal	August 2021
Current Advances in Burkholderia Vaccines Development Wang, Guanbo; Zarodkiewicz, Paulina; Valvano, Miguel A. Cells, Vol. 9, Issue 12 https://doi.org/10.3390/cells9122671	journal	December 2020
Genomic Features and Insights into the Taxonomy, Virulence, and Benevolence of Plant-Associated Burkholderia Species Mannaa, Mohamed; Park, Inmyoung; Seo, Young-Su International Journal of Molecular Sciences, Vol. 20, Issue 1 https://doi.org/10.3390/ijms20010121	journal	December 2018
Proteogenomics in Aid of Host–Pathogen Interaction Studies: A Bacterial Perspective Fels, Ursula; Gevaert, Kris; Van Damme, Petra Proteomes, Vol. 5, Issue 4 https://doi.org/10.3390/proteomes5040026	journal	October 2017
Incidences, Case Fatality Rates and Epidemiology of Melioidosis Worldwide: A Review Paper Fong, Jing Hong; Pillai, Naganathan; Yap, Christina Gertrude OALib, Vol. 08, Issue 06 https://doi.org/10.4236/oalib.1107537	journal	January 2021
FR901228, a novel antitumor bicyclic depsipeptide produced by chromobacterium violaceum No. 968. I. Taxonomy, fermentation, isolation, physico-chemical and biological properties, and antitumor activity. Ueda, Hirotsugu; Nakajima, Hidenori; Hori, Yasuhiro The Journal of Antibiotics, Vol. 47, Issue 3 https://doi.org/10.7164/antibiotics.47.301	journal	January 1994

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