Genomic Analysis of the Marine Yeast Rhodotorula Sphaerocarpa ETNP2018 Reveals Adaptation to the Open Ocean

Overview

Journal BMC Genomics

Publisher Biomed Central

Specialty Genetics

Date 2023 Nov 21

PMID 37986036

Authors

Dylan M Lane

David L Valentine

Xuefeng Peng

Affiliations

Soon will be listed here.

Abstract

Background: Despite a rising interest in the diversity and ecology of fungi in marine environments, there are few published genomes of fungi isolated from the ocean. The basidiomycetous yeast (unicellular fungus) genus Rhodotorula are prevalent and abundant in the open ocean, and they have been isolated from a wide range of other environments. Many of these environments are nutrient poor, such as the Antarctica and the Atacama deserts, raising the question as to how Rhodotorula yeasts may have adapted their metabolic strategies to optimize survival under low nutrient conditions. In order to understand their adaptive strategies in the ocean, the genome of R. sphaerocarpa ETNP2018 was compared to that of fourteen representative Rhodotorula yeasts, isolated from a variety of environments.

Results: Rhodotorula sphaerocarpa ETNP2018, a strain isolated from the oligotrophic part of the eastern tropical North Pacific (ETNP) oxygen minimum zone (OMZ), hosts the smallest of the fifteen genomes and yet the number of protein-coding genes it possesses is on par with the other strains. Its genome exhibits a distinct reduction in genes dedicated to Major Facilitator Superfamily transporters as well as biosynthetic enzymes. However, its core metabolic pathways are fully conserved. Our research indicates that the selective pressures of the ETNP OMZ favor a streamlined genome with reduced overall biosynthetic potential balanced by a stable set of core metabolisms and an expansion of mechanisms for nutrient acquisition.

Conclusions: In summary, this study offers insights into the adaptation of fungi to the oligotrophic ocean and provides valuable information for understanding the ecological roles of fungi in the ocean.

References

Coleine C, Masonjones S, Onofri S, Selbmann L, Stajich J . Draft Genome Sequence of the Yeast sp. Strain CCFEE 5036, Isolated from McMurdo Dry Valleys, Antarctica. Microbiol Resour Announc. 2020; 9(14). PMC: 7118180. DOI: 10.1128/MRA.00020-20. View

Wang M, Mao W, Wang X, Li F, Wang J, Chi Z . Efficient simultaneous production of extracellular polyol esters of fatty acids and intracellular lipids from inulin by a deep-sea yeast Rhodotorula paludigena P4R5. Microb Cell Fact. 2019; 18(1):149. PMC: 6720868. DOI: 10.1186/s12934-019-1200-3. View

Stanke M, Diekhans M, Baertsch R, Haussler D . Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics. 2008; 24(5):637-44. DOI: 10.1093/bioinformatics/btn013. View

Touchette D, Altshuler I, Gostincar C, Zalar P, Raymond-Bouchard I, Zajc J . Novel Antarctic yeast adapts to cold by switching energy metabolism and increasing small RNA synthesis. ISME J. 2021; 16(1):221-232. PMC: 8692454. DOI: 10.1038/s41396-021-01030-9. View

Chew S, Chee W, Than L . The glyoxylate cycle and alternative carbon metabolism as metabolic adaptation strategies of Candida glabrata: perspectives from Candida albicans and Saccharomyces cerevisiae. J Biomed Sci. 2019; 26(1):52. PMC: 6626413. DOI: 10.1186/s12929-019-0546-5. View

Hassett B, Borrego E, Vonnahme T, Rama T, Kolomiets M, Gradinger R . Arctic marine fungi: biomass, functional genes, and putative ecological roles. ISME J. 2019; 13(6):1484-1496. PMC: 6775997. DOI: 10.1038/s41396-019-0368-1. View

Siverio J . Assimilation of nitrate by yeasts. FEMS Microbiol Rev. 2002; 26(3):277-84. DOI: 10.1111/j.1574-6976.2002.tb00615.x. View

Bruna T, Hoff K, Lomsadze A, Stanke M, Borodovsky M . BRAKER2: automatic eukaryotic genome annotation with GeneMark-EP+ and AUGUSTUS supported by a protein database. NAR Genom Bioinform. 2021; 3(1):lqaa108. PMC: 7787252. DOI: 10.1093/nargab/lqaa108. View

Gilbert J, Fagan W . Contrasting mechanisms of proteomic nitrogen thrift in Prochlorococcus. Mol Ecol. 2010; 20(1):92-104. DOI: 10.1111/j.1365-294X.2010.04914.x. View

10.

Cohen A, Nelson H, Nelson N . The family of SMF metal ion transporters in yeast cells. J Biol Chem. 2000; 275(43):33388-94. DOI: 10.1074/jbc.M004611200. View

11.

Kriventseva E, Kuznetsov D, Tegenfeldt F, Manni M, Dias R, Simao F . OrthoDB v10: sampling the diversity of animal, plant, fungal, protist, bacterial and viral genomes for evolutionary and functional annotations of orthologs. Nucleic Acids Res. 2018; 47(D1):D807-D811. PMC: 6323947. DOI: 10.1093/nar/gky1053. View

12.

Giovannoni S, Tripp H, Givan S, Podar M, Vergin K, Baptista D . Genome streamlining in a cosmopolitan oceanic bacterium. Science. 2005; 309(5738):1242-5. DOI: 10.1126/science.1114057. View

13.

Zheng L, Zhai W . Excess nitrogen in the Bohai and Yellow seas, China: Distribution, trends, and source apportionment. Sci Total Environ. 2021; 794:148702. DOI: 10.1016/j.scitotenv.2021.148702. View

14.

Hagestad O, Hou L, Andersen J, Hansen E, Altermark B, Li C . Genomic characterization of three marine fungi, including Emericellopsis atlantica sp. nov. with signatures of a generalist lifestyle and marine biomass degradation. IMA Fungus. 2021; 12(1):21. PMC: 8351168. DOI: 10.1186/s43008-021-00072-0. View

15.

Lu S, Wang J, Chitsaz F, Derbyshire M, Geer R, Gonzales N . CDD/SPARCLE: the conserved domain database in 2020. Nucleic Acids Res. 2019; 48(D1):D265-D268. PMC: 6943070. DOI: 10.1093/nar/gkz991. View

16.

Cantalapiedra C, Hernandez-Plaza A, Letunic I, Bork P, Huerta-Cepas J . eggNOG-mapper v2: Functional Annotation, Orthology Assignments, and Domain Prediction at the Metagenomic Scale. Mol Biol Evol. 2021; 38(12):5825-5829. PMC: 8662613. DOI: 10.1093/molbev/msab293. View

17.

Kastanos E, Woldman Y, Appling D . Role of mitochondrial and cytoplasmic serine hydroxymethyltransferase isozymes in de novo purine synthesis in Saccharomyces cerevisiae. Biochemistry. 1997; 36(48):14956-64. DOI: 10.1021/bi971610n. View

18.

Battaglia E, Benoit I, van den Brink J, Wiebenga A, Coutinho P, Henrissat B . Carbohydrate-active enzymes from the zygomycete fungus Rhizopus oryzae: a highly specialized approach to carbohydrate degradation depicted at genome level. BMC Genomics. 2011; 12:38. PMC: 3032700. DOI: 10.1186/1471-2164-12-38. View

19.

Grzymski J, Dussaq A . The significance of nitrogen cost minimization in proteomes of marine microorganisms. ISME J. 2011; 6(1):71-80. PMC: 3246230. DOI: 10.1038/ismej.2011.72. View

20.

Mannazzu I, Landolfo S, Lopes da Silva T, Buzzini P . Red yeasts and carotenoid production: outlining a future for non-conventional yeasts of biotechnological interest. World J Microbiol Biotechnol. 2015; 31(11):1665-73. DOI: 10.1007/s11274-015-1927-x. View