Transcriptional profile reveals the physiological responses to prey availability in the mixotrophic chrysophyte Poterioochromonas malhamensis

Mingyang Ma; Wentao Yang; Hong Chen; Wanwan Ke; Yingchun Gong; Qiang Hu

doi:10.3389/fmicb.2023.1173541

Transcriptional profile reveals the physiological responses to prey availability in the mixotrophic chrysophyte Poterioochromonas malhamensis

Front Microbiol. 2023 Oct 4:14:1173541. doi: 10.3389/fmicb.2023.1173541. eCollection 2023.

Authors

Mingyang Ma¹, Wentao Yang², Hong Chen^{3

4}, Wanwan Ke⁵, Yingchun Gong⁵, Qiang Hu^{3

4}

Affiliations

¹ Institute for Advanced Study, Shenzhen University, Shenzhen, China.
² Department of Biochemistry and Molecular Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, United States.
³ Faculty of Synthetic Biology, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, China.
⁴ CAS Key Laboratory of Quantitative Engineering Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, China.
⁵ State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, China.

Abstract

Mixotrophic flagellates, which have diverse nutritional modes and play important roles in connecting the microbial loop with the classical food chain, are ideal models to study the mechanisms of adaptation between different nutritional modes in protists. In their natural ecosystems, mixotrophic flagellates may encounter microalgal prey of different digestibility, which may affect the carbon flow. To date, a molecular biological view of the metabolic processes in the mixotrophic flagellate Poterioochromonas malhamensis during nutritional adaptation and feeding on microalgal prey of different digestibility is still lacking. Accordingly, this study focused on the gene expression differences in P. malhamensis under autotrophy, being fed by the digestible microalga Chlorella sorokiniana GT-1, and being fed by the indigestible microalga C. sorokiniana CMBB-146. Results showed that the growth rate of P. malhamensis under autotrophy was much lower than that when fed by digestible microalgae. Addition of C. sorokiniana CMBB-146 could only increase the growth rate of P. malhamensis in the first 3 days, but the cell concentration of P. malhamensis started to decrease gradually after 4 days. Compared to autotrophic P. malhamensis, total 6,583 and 3,510 genes were significantly and differentially expressed in P. malhamensis fed by digestible microalgae and indigestible microalgae, respectively. Compared to autotrophic cells, genes related to the ribosome, lysosome, glycolysis, gluconeogenesis, TCA cycle, β-oxidation, duplication, and β-1,3-glucan in P. malhamensis grazing on digestible prey were up-regulated, while genes related to light harvesting and key enzymes referring to chlorophyll were down-regulated. Genes related to apoptosis and necrosis in P. malhamensis were up-regulated after grazing on indigestible microalgae compared to the autotrophic group, which we suggest is associated with the up-regulation of genes related to lysosome enzymes. This study provides abundant information on the potential intracellular physiological responses of P. malhamensis during the process of nutritional adaptation.

Keywords: Poterioochromonas malhamensis; feeding behavior; physiology; prey availability; transcriptome.

Grants and funding

This work was funded by the National Natural Science Foundation of China (nos. 32002413, 31872201, and 31772419), China Postdoctoral Science Foundation (no. 2019M662749), and the National Key Research and Development Program of China (no. 2018YFD0901504).