Addressing genome scale design tradeoffs in Pseudomonas putida for bioconversion of an aromatic carbon source

Banerjee, Deepanwita; Menasalvas, Javier; Chen, Yan; Gin, Jennifer W.; Baidoo, Edward K.; Petzold, Christopher J.; Eng, Thomas; Mukhopadhyay, Aindrila

doi:10.1038/s41540-024-00480-z

Title: Addressing genome scale design tradeoffs in Pseudomonas putida for bioconversion of an aromatic carbon source

Journal Article · 13 January 2025 · npj Systems Biology and Applications

DOI: https://doi.org/10.1038/s41540-024-00480-z · OSTI ID:2500415

Banerjee, Deepanwita ^[1]; Menasalvas, Javier ^[1]; Chen, Yan ^[1]; Gin, Jennifer W. ^[1]; Baidoo, Edward K. ^[1];

^[1];

^[1]

Joint BioEnergy Institute (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Genome-scale metabolic models (GSMM) are commonly used to identify gene deletion sets that result in growth coupling and pairing product formation with substrate utilization and can improve strain performance beyond levels typically accessible using traditional strain engineering approaches. However, sustainable feedstocks pose a challenge due to incomplete high-resolution metabolic data for non-canonical carbon sources required to curate GSMM and identify implementable designs. Here we address a four-gene deletion design in the Pseudomonas putida KT2440 strain for the lignin-derived non-sugar carbon source, p-coumarate (p-CA), that proved challenging to implement. We examine the performance of the fully implemented design for p-coumarate to glutamine, a useful biomanufacturing intermediate. In this study glutamine is then converted to indigoidine, an alternative sustainable pigment and a model heterologous product that is commonly used to colorimetrically quantify glutamine concentration. Through proteomics, promoter-variation, and growth characterization of a fully implemented gene deletion design, we provide evidence that aromatic catabolism in the completed design is rate-limited by fumarase hydratase (FUM) enzyme activity in the citrate cycle and requires careful optimization of another fumarate hydratase protein (PP_0897) expression to achieve growth and production. A double sensitivity analysis also confirmed a strict requirement for fumarate hydratase activity in the strain where all genes in the growth coupling design have been implemented. Metabolic cross-feeding experiments were used to examine the impact of complete removal of the fumarase hydratase reaction and revealed an unanticipated nutrient requirement, suggesting additional functions for this enzyme. While a complete implementation of the design was achieved, this study highlights the challenge of completely inactivating metabolic reactions encoded by under-characterized proteins, especially in the context of multi-gene edits.

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Research Organization:: Joint BioEnergy Institute (JBEI), Emeryville, CA (United States); LLawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

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

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2500415

Journal Information:: npj Systems Biology and Applications, Journal Name: npj Systems Biology and Applications Journal Issue: 1 Vol. 11; ISSN 2056-7189

Publisher:: Springer NatureCopyright Statement

Country of Publication:: United States

Language:: English

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