An axenic strain reveals the responses of <italic style="font-style: italic">Phaeodactylum tricornutum</italic> to external organic carbon

Zhengfeng ZHU; Zhichao HE; Jian LI; Chengxu ZHOU; Yanrong LI; Lin ZHANG; Xiaohui LI; Spiros N. AGATHOS; Jichang HAN

doi:10.1007/s00343-024-3251-5

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An axenic strain reveals the responses of Phaeodactylum tricornutum to external organic carbon

Biology | Updated：2024-11-19

- An axenic strain reveals the responses of Phaeodactylum tricornutum to external organic carbon
- Journal of Oceanology and Limnology Vol. 42, Issue 5, Pages: 1621-1633(2024)
- Affiliations：
  
  1.College of Food and Pharmaceutical Sciences, Ningbo University, Ningbo315832, China
  2.School of Biological and Chemical Engineering, Panzhihua University, Panzhihua617000, China
  3.Ningbo Institute of Oceanography, Ningbo315832, China
  4.School of Marine Life, Ningbo University, Ningbo315832, China
  5.Earth & Life Institute, Catholic University of Louvain, Louvain-La-Neuve 1348, Belgium
- Author bio：
  
  hanjichang@nbu.edu.cn
- Funds：
- DOI：10.1007/s00343-024-3251-5
  CLC：
- Received：05 December 2023，
  
  Online First：04 January 2024，
  
  Published：01 September 2024
- Accepted：
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ZHU Zhengfeng,HE Zhichao,LI Jian,et al.An axenic strain reveals the responses of Phaeodactylum tricornutum to external organic carbon[J].Journal of Oceanology and Limnology,2024,42(05):1621-1633.
DOI：

ZHU Zhengfeng,HE Zhichao,LI Jian,et al.An axenic strain reveals the responses of Phaeodactylum tricornutum to external organic carbon[J].Journal of Oceanology and Limnology,2024,42(05):1621-1633. DOI： 10.1007/s00343-024-3251-5.

摘要

Abstract

The model diatom

Phaeodactylum

tricornutum

is considered a promising source of various high value bioproducts

and developing cultivation processes is crucial for its commercialization. Although mixotrophy and heterotrophy have been recommended as effective strategies for microalgal cultivation

previous studies on

tricornutum

have yielded conflicting results in terms of cultivating this microalga. To verify the capacity of this microalga utilizing extern

al organic carbon

both heterotrophic and mixotrophic cultivation with varied carbon sources were performed using an axenic strain. The results demonstrate that glycerol was the only organic carbon that substantially stimulated the growth of

tricornutum

in the presence of light. Sodium acetate (NaAc) at low concentrations could also promote growth

while at high concentrations led to severe inhibition under mixotrophic conditions. The addition of glucose imposed no appreciable impact on either cell density or biomass concentration

confirming that

tricornutum

cannot metabolize external glucose. Subsequently

a comparative analysis between mixotrophy and autotrophy was performed to reveal the influences of glycerol on the cellular metabolism based on growth performances

biochemical compositions

and chlorophyll fluorescence parameters. Results also indicate that the addition of glycerol did not have detrimental effects on the capacity of either pigments biosynthesis or photosynthesis

but enhanced the saturated fatty acids and reduced the unsaturated fatty acids.

关键词

Keywords

references

Abu-Ghosh S , Fixler D , Dubinsky Z et al . 2016 . Flashing light in microalgae biotechnology . Bioresource Technology , 203 : 357 - 363 , https://doi.org/10.1016/j.biortech.2015.12.057 https://doi.org/10.1016/j.biortech.2015.12.057 .

Alipanah L , Rohloff J , Winge P et al . 2015 . Whole-cell response to nitrogen deprivation in the diatom Phaeodactylum tricornutum . Journal of Experimental Botany , 66 ( 20 ): 6281 - 6296 , https://doi.org/10.1093/jxb/erv340 https://doi.org/10.1093/jxb/erv340 .

Alipanah L , Winge P , Rohloff J et al . 2018 . Molecular adaptations to phosphorus deprivation and comparison with nitrogen deprivation responses in the diatom Phaeodactylum tricornutum . PLoS One , 13 ( 2 ): e0193335 , https://doi.org/10.1371/journal.pone.0193335 https://doi.org/10.1371/journal.pone.0193335 .

Bligh E G , Dyer W J . 1959 . A rapid method of total lipid extraction and purification . Canadian Journal of Biochemistry and Physiology , 37 ( 8 ): 911 - 917 , https://doi.org/10.1139/o59-099 https://doi.org/10.1139/o59-099 .

Butler T , Kapoore R V , Vaidyanathan S . 2020 . Phaeodactylum tricornutum : a diatom cell factory . Trends in Biotechnology , 38 ( 6 ): 606 - 622 , https://doi.org/10.1016/j.tibtech.2019.12.023 https://doi.org/10.1016/j.tibtech.2019.12.023 .

Carstensen A , Herdean A , Schmidt S B et al . 2018 . The impacts of phosphorus deficiency on the photosynthetic electron transport chain . Plant Physiology , 177 ( 1 ): 271 - 284 , https://doi.org/10.1104/pp.17.01624 https://doi.org/10.1104/pp.17.01624 .

Castillo T , Ramos D , García-Beltrán T et al . 2021 . Mixotrophic cultivation of microalgae: an alternative to produce high-value metabolites . Biochemical Engineering Journal , 176 : 108183 , https://doi.‍org/10.1016/j.bej.2021.108183 https://doi.‍org/10.1016/j.bej.2021.108183 . https://do 10.1016/j.bej.2021.108183 http://dx.doi.org/10.1016/j.bej.2021.108183

Celi C , Fino D , Savorani F . 2022 . Phaeodactylum tricornutum as a source of value-added products: a review on recent developments in cultivation and extraction technologies . Bioresource Technology Reports , 19 : 101122 , https://doi.org/10.1016/j.biteb.2022.101122 https://doi.org/10.1016/j.biteb.2022.101122 .

Cerón-García M C , Fernández-Sevilla J M , Sánchez-Mirón A et al . 2013 . Mixotrophic growth of Phaeodactylum tricornutum on fructose and glycerol in fed-batch and semi-continuous modes . Bioresource Technology , 147 : 569 - 576 , https://doi.org/10.1016/j.biortech.2013.08.092 https://doi.org/10.1016/j.biortech.2013.08.092 .

Chen G Q , Chen F . 2006 . Growing phototrophic cells without light . Biotechnology Letters , 28 ( 9 ): 607 - 616 , https://doi.org/10.1007/s10529-006-0025-4 https://doi.org/10.1007/s10529-006-0025-4 .

Dechatiwongse P , Choorit W . 2021 . Mixotrophic growth of astaxanthin-rich alga haematococcus pluvialis using refined crude glycerol as carbon substrate: batch and fed-batch cultivations . Walailak Journal of Science and Technology (WJST) , 18 ( 2 ): 7354 , https://doi.org/10.48048/wjst.2021.7354 https://doi.org/10.48048/wjst.2021.7354 .

DuBois M , Gilles K A , Hamilton J K et al . 1956 . Colorimetric method for determination of sugars and related substances . Analytical Chemistry , 28 ( 3 ): 350 - 356 , https://doi.org/10.1021/ac60111a017 https://doi.org/10.1021/ac60111a017 .

Figueroa F L , Celis-Plá P S M , Martínez B et al . 2019 . Yield losses and electron transport rate as indicators of thermal stress in Fucus serratus (Ochrophyta) . Algal Research , 41 : 101560 , https://doi.org/10.1016/j.algal.2019.101560 https://doi.org/10.1016/j.algal.2019.101560 .

García M C C , Mirón A S , Sevilla J M F et al . 2005 . Mixotrophic growth of the microalga Phaeodactylum tricornutum : influence of different nitrogen and organic carbon sources on productivity and biomass composition . Process Biochemistry , 40 ( 1 ): 297 - 305 , https://doi.‍org/10.1016/j.procbio.2004.01.016 https://doi.‍org/10.1016/j.procbio.2004.01.016 . https://do 10.1016/j.procbio.2004.01.016 http://dx.doi.org/10.1016/j.procbio.2004.01.016

Hamilton M L , Powers S , Napier J A et al . 2016 . Heterotrophic production of omega-3 long-chain polyunsaturated fatty acids by trophically converted marine diatom Phaeodactylum tricornutum . Marine Drugs , 14 ( 3 ): 53 , https://doi.org/10.3390/md14030053 https://doi.org/10.3390/md14030053 .

Han J C , Wang S , Zhang L et al . 2016a . A method of batch-purifying microalgae with multiple antibiotics at extremely high concentrations . Chinese Journal of Oceanology and Limnology , 34 ( 1 ): 79 - 85 , https://doi.‍org/10.1007/s00343-015-4288-2 https://doi.‍org/10.1007/s00343-015-4288-2 .

Han J C , Zhang L , Wang S et al . 2016b . Co-culturing bacteria and microalgae in organic carbon containing medium . Journal of Biological Research-Thessaloniki , 23 ( 1 ): 8 , https://doi.org/10.1186/s40709-016-0047-6 https://doi.org/10.1186/s40709-016-0047-6 .

Hayward J . 1968 . Studies on the growth of Phaeodaetylum tricornutum . Physiologia Plantarum , 21 ( 1 ): 100 - 108 , https://doi.org/10.1111/j.1399-3054.1968.tb07234.x https://doi.org/10.1111/j.1399-3054.1968.tb07234.x .

Hu J J , Nagarajan D , Zhang Q G et al . 2018 . Heterotrophic cultivation of microalgae for pigment production: a review . Biotechnology Advances , 36 ( 1 ): 54 - 67 , https://doi.org/10.1016/j.biotechadv.2017.09.009 https://doi.org/10.1016/j.biotechadv.2017.09.009 .

Huang B , Marchand J , Blanckaert V et al . 2019 . Nitrogen and phosphorus limitations induce carbon partitioning and membrane lipid remodelling in the marine diatom Phaeodactylum tricornutum . European Journal of Phycology , 54 ( 3 ): 342 - 358 , https://doi.org/10.1080/09670262.2019.1567823 https://doi.org/10.1080/09670262.2019.1567823 .

Ikaran Z , Suárez-Alvarez S , Urreta I et al . 2015 . The effect of nitrogen limitation on the physiology and metabolism of chlorella vulgaris var L3 . Algal Research , 10 : 134 - 144 , https://doi.org/10.1016/j.algal.2015.04.023 https://doi.org/10.1016/j.algal.2015.04.023 .

Kadalag N L , Pawar P R , Prakash G . 2022 . Co-cultivation of Phaeodactylum tricornutum and Aurantiochytrium limacinum for polyunsaturated omega-3 fatty acids production . Bioresource Technology , 346 : 126544 , https://doi.org/10.1016/j.biortech.2021.126544 https://doi.org/10.1016/j.biortech.2021.126544 .

Kim Y , Lama S , Agrawal D et al . 2021 . Acetate as a potential feedstock for the production of value-added chemicals: metabolism and applications . Biotechnology Advances , 49 : 107736 , https://doi.org/10.1016/j.biotechadv.2021.107736 https://doi.org/10.1016/j.biotechadv.2021.107736 .

Krämer L C , Wasser D , Haitz F et al . 2022 . Heterologous expression of HUP1 glucose transporter enables low-light mediated growth on glucose in Phaeodactylum tricornutum . Algal Research , 64 : 102719 , https://doi.‍org/10.1016/j.algal.2022.102719 https://doi.‍org/10.1016/j.algal.2022.102719 . https://do 10.1016/j.algal.2022.102719 http://dx.doi.org/10.1016/j.algal.2022.102719

Li D , Liu R Q , Cui X Y et al . 2021 . Co-culture of bacteria and microalgae for treatment of high concentration biogas slurry . Journal of Water Process Engineering , 41 : 102014 , https://doi.org/10.1016/j.jwpe.2021.102014 https://doi.org/10.1016/j.jwpe.2021.102014 .

Li Y T , Han D X , Sommerfeld M et al . 2011 . Photosynthetic carbon partitioning and lipid production in the oleaginous microalga Pseudochlorococcum sp. (Chlorophyceae) under nitrogen-limited conditions . Bioresource Technology , 102 ( 1 ): 123 - 129 , https://doi.org/10.1016/j.biortech.2010.06.036 https://doi.org/10.1016/j.biortech.2010.06.036 .

Liu X J , Duan S S , Li A F et al . 2009a . Effects of glycerol on the fluorescence spectra and chloroplast ultrastruc ture of Phaeodactylum tricornutum (Bacillariophyta) . Journal of Integrative Plant Biology , 51 ( 3 ): 272 - 278 , https://doi.org/10.1111/j.1744-7909.2008.00767.x https://doi.org/10.1111/j.1744-7909.2008.00767.x .

Liu X J , Duan S S , Li A F et al . 2009b . Effects of organic carbon sources on growth, photosynthesis, and respiration of Phaeodactylum tricornutum . Journal of Applied Phycology , 21 ( 2 ): 239 - 246 , https://doi.org/10.1007/s10811-008-9355-z https://doi.org/10.1007/s10811-008-9355-z .

Marella T K , Bhattacharjya R , Tiwari A . 2021 . Impact of organic carbon acquisition on growth and functional biomolecule production in diatoms . Microbial Cell Factories , 20 ( 1 ): 135 , https://doi.org/10.1186/s12934-021-01627-x https://doi.org/10.1186/s12934-021-01627-x .

Msanne J , Xu D , Konda A R et al . 2012 . Metabolic and gene expression changes triggered by nitrogen deprivation in the photoautotrophically grown microalgae Chlamydomonas reinhardtii and Coccomyxa sp. C-169 . Phytochemistry , 75 : 50 - 59 , https://doi.org/10.1016/j.phytochem.2011.12.007 https://doi.org/10.1016/j.phytochem.2011.12.007 .

Patel A , Matsakas L , Hrůzová K et al . 2019 . Biosynthesis of nutraceutical fatty acids by the oleaginous marine microalgae Phaeodactylum tricornutum utilizing hydrolysates from organosolv-pretreated birch and spruce biomass . Marine Drugs , 17 ( 2 ): 119 , https://doi.org/10.3390/md17020119 https://doi.org/10.3390/md17020119 .

Penhaul Smith J K , Hughes A D , McEvoy L et al . 2020 . Tailoring of the biochemical profiles of microalgae by employing mixotrophic cultivation . Bioresource Technology Reports , 9 : 100321 , https://doi.org/10.1016/j.biteb.2019.100321 https://doi.org/10.1016/j.biteb.2019.100321 .

Perera I A , Abinandan S , Panneerselvan L et al . 2022 . Co-culturing of microalgae and bacteria in real wastewaters alters indigenous bacterial communities enhancing effluent bioremediation . Algal Research , 64 : 102705 , https://doi.org/10.1016/j.algal.2022.102705 https://doi.org/10.1016/j.algal.2022.102705 .

Perez-Garcia O , Escalante F M E , de-Bashan L E et al . 2011 . Heterotrophic cultures of microalgae: metabolism and potential products . Water Research , 45 ( 1 ): 11 - 36 , https://doi.org/10.1016/j.watres.2010.08.037 https://doi.org/10.1016/j.watres.2010.08.037 .

Poddar N , Sen R , Martin G J O . 2018 . Glycerol and nitrate utilisation by marine microalgae Nannochloropsis salina and Chlorella sp. and associated bacteria during mixotrophic and heterotrophic growth . Algal Research , 33 : 298 - 309 , https://doi.org/10.1016/j.algal.2018.06.002 https://doi.org/10.1016/j.algal.2018.06.002 .

Sajjadi B , Chen W Y , Raman A A A et al . 2018 . Microalgae lipid and biomass for biofuel production: a comprehensive review on lipid enhancement strategies and their effects on fatty acid composition . Renewable and Sustainable Energy Reviews , 97 : 200 - 232 , https://doi.org/10.1016/j.rser.2018.07.050 https://doi.org/10.1016/j.rser.2018.07.050 .

Sedmak J J , Grossberg S E . 1977 . A rapid, sensitive, and versatile assay for protein using Coomassie brilliant blue G250 . Analytical Biochemistry , 79 ( 1-2 ): 544 - 552 , https://doi.org/10.1016/0003-2697(77)90428-6 https://doi.org/10.1016/0003-2697(77)90428-6 .

Song Z D , Lye G J , Parker B M . 2020 . Morphological and biochemical changes in Phaeodactylum tricornutum triggered by culture media: implications for industrial exploitation . Algal Research , 47 : 101822 , https://doi.‍org/10.1016/j.algal.2020.101822 https://doi.‍org/10.1016/j.algal.2020.101822 . https://do 10.1016/j.algal.2020.101822 http://dx.doi.org/10.1016/j.algal.2020.101822

Su M , D'Imporzano G , Veronesi D et al . 2020 . Phaeodactylum tricornutum cultivation under mixotrophic conditions with glycerol supplied with ultrafiltered digestate: a simple biorefinery approach recovering C and N . Journal of Biotechnology , 323 : 73 - 81 , https://doi.org/10.1016/j.jbiotec.2020.07.018 https://doi.org/10.1016/j.jbiotec.2020.07.018 .

Sun Y , Xin Y , Zhang L Y et al . 2022 . Enhancement of violaxanthin accumulation in Nannochloropsis oceanica by overexpressing a carotenoid isomerase gene from Phaeodactylum tricornutum . Frontiers in Microbiology , 13 : 942883 , https://doi.org/10.3389/fmicb.2022.942883 https://doi.org/10.3389/fmicb.2022.942883 .

Tan L J , Xu W J , He X L et al . 2019 . The feasibility of F v / F m on judging nutrient limitation of marine algae through indoor simulation and in situ experiment . Estuarine, Coastal and Shelf Science , 229 : 106411 , https://doi.org/10.1016/j.ecss.2019.106411 https://doi.org/10.1016/j.ecss.2019.106411 .

Villanova V , Fortunato A E , Singh D et al . 2017 . Investigating mixotrophic metabolism in the model diatom Phaeodactylum tricornutum . Philosophical Transactions of the Royal Society B : Biological Sciences , 372 ( 1728 ): 20160404 , https://doi.org/10.1098/rstb.2016.0404 https://doi.org/10.1098/rstb.2016.0404 .

Villanova V , Singh D , Pagliardini J et al . 2021 . Boosting biomass quantity and quality by improved mixotrophic culture of the diatom Phaeodactylum tricornutum . Frontiers in Plant Science , 12 : 642199 , https://doi.org/10.3389/fpls.2021.642199 https://doi.org/10.3389/fpls.2021.642199 .

Wang H Y , Fu R , Pei G F . 2012 . A study on lipid production of the mixotrophic microalgae Phaeodactylum tricornutum on various carbon sources . African Journal of Microbiology Research , 6 ( 5 ): 1041 - 1047 , https://doi.org/10.5897/ajmr11.1365 https://doi.org/10.5897/ajmr11.1365 .

Wang S , Wu S , Yang G P et al . 2021 . A review on the progress, challenges and prospects in commercializing microalgal fucoxanthin . Biotechnology Advances , 53 : 107865 , https://doi.org/10.1016/j.biotechadv.2021.107865 https://doi.org/10.1016/j.biotechadv.2021.107865 .

Wang S , Zhou X Y , Wu S et al . 2023 . Transcriptomic and metabolomic analyses revealed regulation mechanism of mixotrophic Cylindrotheca sp. glycerol utilization and biomass promotion . Biotechnology for Biofuels and Bioproducts , 16 ( 1 ): 84 , https://doi.‍org/10.1186/s13068-023-02338-8 https://doi.‍org/10.1186/s13068-023-02338-8 . https://do 10.1186/s13068-023-02338-8 http://dx.doi.org/10.1186/s13068-023-02338-8

Yang Z K , Niu Y F , Ma Y H et al . 2013 . Molecular and cellular mechanisms of neutral lipid accumulation in diatom following nitrogen deprivation . Biotechnology for Biofuels , 6 ( 1 ): 67 , https://doi.‍org/10.1186/1754-6834-6-67 https://doi.‍org/10.1186/1754-6834-6-67 . https://do 10.1186/1754-6834-6-67 http://dx.doi.org/10.1186/1754-6834-6-67

Young E B , Beardall J . 2003 . Photosynthetic function in Dunaliella tertiolecta (Chlorophyta) during a nitrogen starvation and recovery cycle . Journal of Phycology , 39 ( 5 ): 897 - 905 , https://doi.org/10.1046/j.1529-8817.2003.03042.x https://doi.org/10.1046/j.1529-8817.2003.03042.x .

Zaslavskaia L A , Lippmeier J C , Shih C et al . 2001 . Trophic conversion of an obligate photoautotrophic organism through metabolic engineering . Science , 292 ( 5524 ): 2073 - 2075 , https://doi.org/10.1126/science.160015 https://doi.org/10.1126/science.160015 .

Zhang L , Wang S , Han J C et al . 2022 . Manipulation of triacylglycerol biosynthesis in Nannochloropsis oceanica by overexpressing an Arabidopsis thaliana diacylglycerol acyltransferase gene . Algal Research , 61 : 102590 , https://doi.org/10.1016/j.algal.2021.102590 https://doi.org/10.1016/j.algal.2021.102590 .

Zhang L , Yang S P , Xu J L et al . 2020 . Application of exogenous salicylic acid on improving high temperature resistance of Nannochloropsis oceanica . Aquaculture International , 28 ( 6 ): 2235 - 2246 , https://doi.‍org/10.1007/s10499-020-00592-3 https://doi.‍org/10.1007/s10499-020-00592-3 . https://do 10.1007/s10499-020-00592-3 http://dx.doi.org/10.1007/s10499-020-00592-3

Zhang W L , Zhou W J , Jiang S et al . 2023 . Heterotrophic modification of Phaeodactylum tricornutum Bohlin . Algal Research , 72 : 103137 , https://doi.org/10.1016/j.algal.2023.103137 https://doi.org/10.1016/j.algal.2023.103137 .

Zhao L S , Li K , Wang Q M et al . 2017 . Nitrogen starvation impacts the photosynthetic performance of Porphyridium cruentum as revealed by chlorophyll a fluorescence . Scientific Reports , 7 ( 1 ): 8542 , https://doi.org/10.1038/s41598-017-08428-6 https://doi.org/10.1038/s41598-017-08428-6 .

Zheng Y T , Quinn A H , Sriram G . 2013 . Experimental evidence and isotopomer analysis of mixotrophic glucose metabolism in the marine diatom Phaeodactylum tricornutum . Microbial Cell Factories , 12 ( 1 ): 109 , https://doi.org/10.1186/1475-2859-12-109 https://doi.org/10.1186/1475-2859-12-109 .

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Related Author

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Related Institution

Laboratory of Marine Organism Taxonomy and Phylogeny, Institute of Oceanology, Chinese Academy of Sciences

College of Food Science and Engineering, Ningbo University

Key Laboratory of Applied Marine Biotechnology, Ministry of Education of China, Ningbo University

Earth Life Institute, Bioengineering Laboratory, Catholic University of Louvain, Louvain- -Neuve

Qingdao Innovation and Development Base, Harbin Engineering University

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⁰

An axenic strain reveals the responses of Phaeodactylum tricornutum to external organic carbon

DOI：10.1007/s00343-024-3251-5

摘要

Abstract

关键词

Keywords

references