A transcriptomic atlas of acute stress response to low pH in multiple Issatchenkia orientalis strains

Dubinkina, Veronika; Bhogale, Shounak; Hsieh, Ping-Hung; Dibaeinia, Payam; Nambiar, Ananthan; Maslov, Sergei; Yoshikuni, Yasuo; Sinha, Saurabh

doi:10.1128/spectrum.02536-23

A transcriptomic atlas of acute stress response to low pH in multiple Issatchenkia orientalis strains

Journal Article · Wed Nov 29 00:00:00 EST 2023 · Microbiology Spectrum

DOI:https://doi.org/10.1128/spectrum.02536-23· OSTI ID:2309742

^[1]; Bhogale, Shounak ^[2]; ^[3]; Dibaeinia, Payam ^[2]; Nambiar, Ananthan ^[2]; ^[2]; ^[4]; ^[5]

Univ. of Illinois at Urbana-Champaign, IL (United States); Gladstone Institute of Data Science and Biotechnology, San Francisco, CA (United States); University of Illinois Urbana-Champaign
Univ. of Illinois at Urbana-Champaign, IL (United States)
Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Hokkaido Univ. (Japan); Tokyo University of Agriculture and Technology (Japan)
Univ. of Illinois at Urbana-Champaign, IL (United States); Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States); Georgia Institute of Technology, Atlanta, GA (United States); Emory Univ., Atlanta, GA (United States)

Because of its natural stress tolerance to low pH, Issatchenkia orientalis (a.k.a. Pichia kudriavzevii) is a promising non-model yeast for bio-based production of organic acids. Yet, this organism is relatively unstudied, and specific mechanisms of its tolerance to low pH are poorly understood, limiting commercial use. In this study, we selected 12 I. orientalis strains with varying acid stress tolerance (six tolerant and six susceptible) and profiled their transcriptomes in different pH conditions to study potential mechanisms of pH tolerance in this species. We identified hundreds of genes whose expression response is shared by tolerant strains but not by susceptible strains, or vice versa, as well as genes whose responses are reversed between tolerant and susceptible strains. We mapped regulatory mechanisms of transcriptomic responses via motif analysis as well as differential network reconstruction, identifying several transcription factors, including Stb5, Mac1, and Rtg1/Rtg3, some of which are known for their roles in acid response in Saccharomyces cerevisiae. Functional genomics analysis of short-listed genes and transcription factors suggested significant roles for energy metabolism and translation-related processes, as well as the cell wall integrity pathway and RTG-dependent retrograde signaling pathway. Finally, we conducted additional experiments for two organic acids, 3-hydroxypropionate and citramalate, to eliminate acid-specific effects and found potential roles for glycolysis and trehalose biosynthesis specifically for response to low pH. In summary, our approach of comparative transcriptomics and phenotypic contrasting, along with a multi-pronged bioinformatics analysis, suggests specific mechanisms of tolerance to low pH in I. orientalis that merit further validation through experimental perturbation and engineering.

View Accepted Manuscript (DOE)

Research Organization:: Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States); Univ. of Illinois at Urbana-Champaign, IL (United States)

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

Grant/Contract Number:: AC02-05CH11231; SC0018420

OSTI ID:: 2309742

Journal Information:: Microbiology Spectrum, Journal Name: Microbiology Spectrum Journal Issue: 1 Vol. 12; ISSN 2165-0497

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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