Non-canonical d-xylose and l-arabinose metabolism via d-arabitol in the oleaginous yeast Rhodosporidium toruloides

Adamczyk, Paul A.; Coradetti, Samuel T.; Gladden, John M.

doi:10.1186/s12934-023-02126-x

Non-canonical d-xylose and l-arabinose metabolism via d-arabitol in the oleaginous yeast Rhodosporidium toruloides

Journal Article · Thu Aug 03 00:00:00 EDT 2023 · Microbial Cell Factories

DOI:https://doi.org/10.1186/s12934-023-02126-x· OSTI ID:1993647

Adamczyk, Paul A.; Coradetti, Samuel T.; Gladden, John M.

Abstract

R. toruloides is an oleaginous yeast, with diverse metabolic capacities and high tolerance for inhibitory compounds abundant in plant biomass hydrolysates. While R. toruloides grows on several pentose sugars and alcohols, further engineering of the native pathway is required for efficient conversion of biomass-derived sugars to higher value bioproducts. A previous high-throughput study inferred that R. toruloides possesses a non-canonical l -arabinose and d -xylose metabolism proceeding through d -arabitol and d -ribulose. In this study, we present a combination of genetic and metabolite data that refine and extend that model. Chiral separations definitively illustrate that d -arabitol is the enantiomer that accumulates under pentose metabolism. Deletion of putative d -arabitol-2-dehydrogenase (RTO4_9990) results in > 75% conversion of d -xylose to d -arabitol, and is growth-complemented on pentoses by heterologous xylulose kinase expression. Deletion of putative d -ribulose kinase (RTO4_14368) arrests all growth on any pentose tested. Analysis of several pentose dehydrogenase mutants elucidates a complex pathway with multiple enzymes mediating multiple different reactions in differing combinations, from which we also inferred a putative l -ribulose utilization pathway. Our results suggest that we have identified enzymes responsible for the majority of pathway flux, with additional unknown enzymes providing accessory activity at multiple steps. Further biochemical characterization of the enzymes described here will enable a more complete and quantitative understanding of R. toruloides pentose metabolism. These findings add to a growing understanding of the diversity and complexity of microbial pentose metabolism.

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Research Organization:: Environmental Molecular Sciences Laboratory (EMSL), Richland, WA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Sandia National Laboratories (SNL-CA), Livermore, CA (United States)

Sponsoring Organization:: USDOE; USDOE National Nuclear Security Administration (NNSA); USDOE Office of Energy Efficiency and Renewable Energy (EERE), Office of Sustainable Transportation. Bioenergy Technologies Office (BETO); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; AC05-76RL01830; NA0003525

OSTI ID:: 1993647

Alternate ID(s):: OSTI ID: 2311350

Report Number(s):: SAND--2023-09655J; 145; PII: 2126

Journal Information:: Microbial Cell Factories, Journal Name: Microbial Cell Factories Journal Issue: 1 Vol. 22; ISSN 1475-2859

Publisher:: Springer Science + Business MediaCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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Functional genomics of lipid metabolism in the oleaginous yeast Rhodosporidium toruloides Coradetti, Samuel T.; Pinel, Dominic; Geiselman, Gina M. eLife, Vol. 7 https://doi.org/10.7554/eLife.32110	journal	March 2018

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59 BASIC BIOLOGICAL SCIENCES
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