Abstract
Objective
Currently, there is lack of a consistent and highly enriched source for docosapentaenoic acid (n-3 DPA, C22:5), and this work report the isolation of microorganism that naturally produces n-3 DPA.
Results
In this work, we screened microorganisms in our culture collections with the goal to isolate a strain with high levels of n-3 DPA. We isolated a strain of Sphaeroforma arctica that produces up to 11% n-3 DPA in total fatty acid and has a high n-3 DPA to DHA/EPA ratio. The cell growth of the isolated strain was characterized using microscopy imaging and flow cytometer technologies to confirm the coenocytic pattern of cell divisions previously described in S. arctica. Our novel isolate of S. arctica grew more robustly and produced significantly more n-3 DPA compared to previously isolated and described strains indicating the uniqueness of the discovered strain.
Conclusion
Overall, this work reports a first isolate n-3 DPA producing microorganism and establishes the foundation for future strain improvement and elucidation of the physiological function of this LC-PUFA for human nutrition and health.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated in this work are available in the manuscript and supplementary data.
References
Apt KE, Warren Behrens P, Milton Hansen J et al. (2015) Eicosapentaenoic acid-producing microorganisms, fatty acid compositions, and methods of making and uses thereof. US Patent.
Aursnes M, Tungen JE, Vik A et al (2014) Total synthesis of the lipid mediator PD1 n-3 DPA : configurational assignments and anti-inflammatory and pro-resolving actions. J Nat Prod 77:910–916. https://doi.org/10.1021/np4009865
Dalli J, Colas RA, Serhan CN (2013) Novel n-3 immunoresolvents: structures and actions. Sci Rep 3:1940. https://doi.org/10.1038/srep01940
Delplanque B, Gibson R, Koletzko B et al (2015) Lipid quality in infant nutrition. J Pediatr Gastroenterol Nutr 61:8–17. https://doi.org/10.1097/MPG.0000000000000818
Drouin G, Rioux V, Legrand P (2019) The n-3 docosapentaenoic acid (DPA): a new player in the n-3 long chain polyunsaturated fatty acid family. Biochimie 159:36–48. https://doi.org/10.1016/j.biochi.2019.01.022
Dudin O, Ondracka A, Grau-Bové X et al (2019) A unicellular relative of animals generates a layer of polarized cells by actomyosin-dependent cellularization. Elife. https://doi.org/10.7554/eLife.49801
Dyall SC (2015) Long-chain omega-3 fatty acids and the brain: a review of the independent and shared effects of EPA, DPA and DHA. Front Aging Neurosci. https://doi.org/10.3389/fnagi.2015.00052
Gemperlein K, Dietrich D, Kohlstedt M et al (2019) Polyunsaturated fatty acid production by Yarrowia lipolytica employing designed myxobacterial PUFA synthases. Nat Commun 10:4055. https://doi.org/10.1038/s41467-019-12025-8
Gold DA, Grabenstatter J, de Mendoza A et al (2016) Sterol and genomic analyses validate the sponge biomarker hypothesis. Proc Natl Acad Sci USA 113:2684–2689. https://doi.org/10.1073/pnas.1512614113
Hamilton ML, Warwick J, Terry A et al (2015) Towards the industrial production of omega-3 long chain polyunsaturated fatty acids from a genetically modified diatom Phaeodactylum tricornutum. PLoS ONE 10:e0144054. https://doi.org/10.1371/journal.pone.0144054
Innes J, Calder P (2018) The differential effects of eicosapentaenoic acid and docosahexaenoic acid on cardiometabolic risk factors: a systematic review. Int J Mol Sci 19:532. https://doi.org/10.3390/ijms19020532
Ishibashi Y, Goda H, Hamaguchi R et al (2021) PUFA synthase-independent DHA synthesis pathway in Parietichytrium sp. and its modification to produce EPA and n-3DPA. Commun Biol 4:1378. https://doi.org/10.1038/s42003-021-02857-w
Jøstensen J-P, Sperstad S, Johansen S, Landfald B (2002) Molecular-phylogenetic, structural and biochemical features of a cold-adapted, marine ichthyosporean near the animal-fungal divergence, described from in vitro cultures. Eur J Protistol 38:93–104. https://doi.org/10.1078/0932-4739-00855
Jovanovic S, Dietrich D, Becker J et al (2021) Microbial production of polyunsaturated fatty acids—high-value ingredients for aquafeed, superfoods, and pharmaceuticals. Curr Opin Biotechnol 69:199–211. https://doi.org/10.1016/j.copbio.2021.01.009
Lang I, Hodac L, Friedl T, Feussner I (2011) Fatty acid profiles and their distribution patterns in microalgae: a comprehensive analysis of more than 2000 strains from the SAG culture collection. BMC Plant Biol 11:124. https://doi.org/10.1186/1471-2229-11-124
Li J, Yin H, Bibus DM, Byelashov OA (2016) The role of omega-3 docosapentaenoic acid in pregnancy and early development. Eur J Lipid Sci Technol 118:1692–1701. https://doi.org/10.1002/ejlt.201600076
Marshall WL, Berbee ML (2013) Comparative morphology and genealogical delimitation of cryptic species of sympatric isolates of Sphaeroforma (Ichthyosporea, Opisthokonta). Protist 164:287–311. https://doi.org/10.1016/j.protis.2012.12.002
Mitani E, Nakayama F, Matsuwaki I et al (2017) Fatty acid composition profiles of 235 strains of three microalgal divisions within the NIES microbial culture collection. Microb Resour Syst 33(1):19–29
Ondracka A, Dudin O, Ruiz-Trillo I (2018) Decoupling of nuclear division cycles and cell size during the coenocytic growth of the Ichthyosporean Sphaeroforma arctica. Curr Biol 28:1964–1969. https://doi.org/10.1016/j.cub.2018.04.074
Pfeifer JWHJMGJRDXDBPWAKE (2017) Eicosapentaenoic Acid - Producing Microorganisms, Fatty Acid Compositions, And Methods Of Making And uses thereof
Rhee JJ, Kim E, Buring JE, Kurth T (2017) Fish consumption, omega-3 fatty acids, and risk of cardiovascular disease. Am J Prev Med 52:10–19. https://doi.org/10.1016/j.amepre.2016.07.020
Richter CK, Bisselou KS, Nordgren TM, Smith L, Appiah AK, Hein N, Anderson-Berry A, Kris-Etherton P, Hanson C, Skulas-Ray AC (2019) n-3 Docosapentaenoic acid intake and relationship with plasma long-chain n-3 fatty acid concentrations in the United States: NHANES 2003–2014. Lipids 54(4):221–230. https://doi.org/10.1002/lipd.12146
Singh A, Ward OP (1998) Docosapentaenoic acid (C22:5, ?-3) production by Pythium acanthicum. J Ind Microbiol Biotechnol 20:187–191. https://doi.org/10.1038/sj.jim.2900505
Suga H, Ruiz-Trillo I (2013) Development of ichthyosporeans sheds light on the origin of metazoan multicellularity. Dev Biol 377:284–292. https://doi.org/10.1016/j.ydbio.2013.01.009
Vrinten P, Mavraganis I, Qiu X, Senger T (2013) Biosynthesis of long chain polyunsaturated fatty acids in the Marine Ichthyosporean Sphaeroforma arctica. Lipids 48:263–274. https://doi.org/10.1007/s11745-012-3738-2
Zhang K, Li H, Chen W et al (2017) Regulation of the docosapentaenoic acid/docosahexaenoic acid ratio (DPA/DHA Ratio) in Schizochytrium limacinum B4D1. Appl Biochem Biotechnol 182:67–81. https://doi.org/10.1007/s12010-016-2311-5
Zhang N, Jin L, Liu C, Zhang R, Siebert H-C, Li Y, Loers G, Petridis AK, Xia Z, Dong H, Zheng X (2021) An antarctic krill oil-based diet elicits neuroprotective effects by inhibiting oxidative stress and rebalancing the M1/M2 microglia phenotype in a cuprizone model for demyelination. J Funct Foods 76:104309. https://doi.org/10.1016/j.jff.2020.104309
Acknowledgements
We would like to thank all dsm-firmenich team members for supporting the project. We would like to special thank support and discussion from Dr. Yao Lu for the analytical methods used in the study, Anita Patel and Mary Lee at Columbia site for carrying out the analytical assays.
Funding
This work was funded internally by dsm-firmenich science and research.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Conceptualization, supervision, and funding acquisition were performed by Ross Zirkle and Oliver May. Material preparation, data collection and analysis were performed by Qiang Yan, Ying Liu, Kelly Haake, Christa Barrett, and Daniel Seeler. The first draft of the manuscript was written by Qiang Yan and Ross Zirkle, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
dsm-fermenich is filing a patent on this work. Any interest can be consulted with Ross Zirkle and Oliver May.
Ethical approval
This article does not contain any studies with human or animal subjects performed by any of the authors.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Yan, Q.W., Liu, YC., Barrett, C. et al. Accumulation of docosapentaenoic acid (n-3 DPA) in a novel isolate of the marine ichthyosporean Sphaeroforma arctica. Biotechnol Lett 46, 373–383 (2024). https://doi.org/10.1007/s10529-024-03472-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10529-024-03472-5