Mixotrophic growth of a ubiquitous marine diatom

. 2024 Jul 19 ; 10 (29) : eado2623. [epub] 20240717

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid39018398

Grantová podpora
P20 GM103446 NIGMS NIH HHS - United States

Diatoms are major players in the global carbon cycle, and their metabolism is affected by ocean conditions. Understanding the impact of changing inorganic nutrients in the oceans on diatoms is crucial, given the changes in global carbon dioxide levels. Here, we present a genome-scale metabolic model (iMK1961) for Cylindrotheca closterium, an in silico resource to understand uncharacterized metabolic functions in this ubiquitous diatom. iMK1961 represents the largest diatom metabolic model to date, comprising 1961 open reading frames and 6718 reactions. With iMK1961, we identified the metabolic response signature to cope with drastic changes in growth conditions. Comparing model predictions with Tara Oceans transcriptomics data unraveled C. closterium's metabolism in situ. Unexpectedly, the diatom only grows photoautotrophically in 21% of the sunlit ocean samples, while the majority of the samples indicate a mixotrophic (71%) or, in some cases, even a heterotrophic (8%) lifestyle in the light. Our findings highlight C. closterium's metabolic flexibility and its potential role in global carbon cycling.

Zobrazit více v PubMed

Y. Matsuda, P. G. Kroth, “Carbon fixation in diatoms” in The Structural Basis of Biological Energy Generation (Springer, 2014; https://link.springer.com/10.1007/978-94-017-8742-0_18), pp. 335–362.

Büchel C., How diatoms harvest light. Science 365, 447–448 (2019). PubMed

Guiry M. D., How many species of algae are there? J. Phycol. 48, 1057–1063 (2012). PubMed

De Tommasi E., Gielis J., Rogato A., Diatom frustule morphogenesis and function: A multidisciplinary survey. Mar. Genomics 35, 1–18 (2017). PubMed

Wang S., Verma S. K., Hakeem Said I., Thomsen L., Ullrich M. S., Kuhnert N., Changes in the fucoxanthin production and protein profiles in Cylindrotheca closterium in response to blue light-emitting diode light. Microb. Cell Fact. 17, 110 (2018). PubMed PMC

Cohen N. R., Mixotrophic plankton foraging behaviour linked to carbon export. Nat. Commun. 13, 1302 (2022). PubMed PMC

Ward B. A., Follows M. J., Marine mixotrophy increases trophic transfer efficiency, mean organism size, and vertical carbon flux. Proc. Natl. Acad. Sci. U.S.A. 113, 2958–2963 (2016). PubMed PMC

Malviya S., Scalco E., Audic S., Vincent F., Veluchamy A., Poulain J., Wincker P., Iudicone D., de Vargas C., Bittner L., Zingone A., Bowler C., Insights into global diatom distribution and diversity in the world’s ocean. Proc. Natl. Acad. Sci. U. S.A. 113, E1516–E1525 (2016). PubMed PMC

Wang H., Robinson J. L., Kocabas P., Gustafsson J., Anton M., Cholley P.-E., Huang S., Gobom J., Svensson T., Uhlen M., Zetterberg H., Nielsen J., Genome-scale metabolic network reconstruction of model animals as a platform for translational research. Proc. Natl. Acad. Sci. U.S.A. 118, e2102344118 (2021). PubMed PMC

Yang J. E., Park S. J., Kim W. J., Kim H. J., Kim B. J., Lee H., Shin J., Lee S. Y., One-step fermentative production of aromatic polyesters from glucose by metabolically engineered Escherichia coli strains. Nat. Commun. 9, 79 (2018). PubMed PMC

Monk J. M., Lloyd C. J., Brunk E., Mih N., Sastry A., King Z., Takeuchi R., Nomura W., Zhang Z., Mori H., Feist A. M., Palsson B. O., iML1515, a knowledgebase that computes Escherichia coli traits. Nat. Biotechnol. 35, 904–908 (2017). PubMed PMC

Monk J. M., Charusanti P., Aziz R. K., Lerman J. A., Premyodhin N., Orth J. D., Feist A. M., Palsson B. Ø., Genome-scale metabolic reconstructions of multiple Escherichia coli strains highlight strain-specific adaptations to nutritional environments. Proc. Natl. Acad. Sci. U.S.A. 110, 20338–20343 (2013). PubMed PMC

Kumar M., Ji B., Zengler K., Nielsen J., Modelling approaches for studying the microbiome. Nat. Microbiol. 4, 1253–1267 (2019). PubMed

Kumar M., Ji B., Babaei P., Das P., Lappa D., Ramakrishnan G., Fox T. E., Haque R., Petri W. A., Bäckhed F., Nielsen J., Gut microbiota dysbiosis is associated with malnutrition and reduced plasma amino acid levels: Lessons from genome-scale metabolic modeling. Metab. Eng. 49, 128–142 (2018). PubMed PMC

Zuñiga C., Li T., Guarnieri M. T., Jenkins J. P., Li C.-T., Bingol K., Kim Y.-M., Betenbaugh M. J., Zengler K., Synthetic microbial communities of heterotrophs and phototrophs facilitate sustainable growth. Nat. Commun. 11, 3803 (2020). PubMed PMC

Levering J., Broddrick J., Dupont C. L., Peers G., Beeri K., Mayers J., Gallina A. A., Allen A. E., Palsson B. O., Zengler K., Genome-scale model reveals metabolic basis of biomass partitioning in a model diatom. PLOS ONE 11, e0155038 (2016). PubMed PMC

Lavoie M., Saint-Béat B., Strauss J., Guérin S., Allard A., Hardy S. V., Falciatore A., Lavaud J., Genome-scale metabolic reconstruction and in silico perturbation analysis of the polar diatom Fragilariopsis cylindrus predicts high metabolic robustness. Biology (Basel). 9, 30 (2020). PubMed PMC

van Tol H. M., Armbrust E. V., Genome-scale metabolic model of the diatom Thalassiosira pseudonana highlights the importance of nitrogen and sulfur metabolism in redox balance. PLOS ONE 16, e0241960 (2021). PubMed PMC

Ahmad A., Tiwari A., Srivastava S., A genome-scale metabolic model of Thalassiosira pseudonana CCMP 1335 for a systems-level understanding of its metabolism and biotechnological potential. Microorganisms 8, 1396 (2020). PubMed PMC

Salazar G., Paoli L., Alberti A., Huerta-Cepas J., Ruscheweyh H.-J., Cuenca M., Field C. M., Coelho L. P., Cruaud C., Engelen S., Gregory A. C., Labadie K., Marec C., Pelletier E., Royo-Llonch M., Roux S., Sánchez P., Uehara H., Zayed A. A., Zeller G., Carmichael M., Dimier C., Ferland J., Kandels S., Picheral M., Pisarev S., Poulain J., Acinas S. G., Babin M., Bork P., Bowler C., de Vargas C., Guidi L., Hingamp P., Iudicone D., Karp-Boss L., Karsenti E., Ogata H., Pesant S., Speich S., Sullivan M. B., Wincker P., Sunagawa S., Acinas S. G., Babin M., Bork P., Boss E., Bowler C., Cochrane G., de Vargas C., Follows M., Gorsky G., Grimsley N., Guidi L., Hingamp P., Iudicone D., Jaillon O., Kandels-Lewis S., Karp-Boss L., Karsenti E., Not F., Ogata H., Pesant S., Poulton N., Raes J., Sardet C., Speich S., Stemmann L., Sullivan M. B., Sunagawa S., Wincker P., Gene expression changes and community turnover differentially shape the global ocean metatranscriptome. Cell 179, 1068–1083.e21 (2019). PubMed PMC

de Vargas C., Audic S., Henry N., Decelle J., Mahé F., Logares R., Lara E., Berney C., Le Bescot N., Probert I., Carmichael M., Poulain J., Romac S., Colin S., Aury J.-M., Bittner L., Chaffron S., Dunthorn M., Engelen S., Flegontova O., Guidi L., Horák A., Jaillon O., Lima-Mendez G., Lukeš J., Malviya S., Morard R., Mulot M., Scalco E., Siano R., Vincent F., Zingone A., Dimier C., Picheral M., Searson S., Kandels-Lewis S., Acinas S. G., Bork P., Bowler C., Gorsky G., Grimsley N., Hingamp P., Iudicone D., Not F., Ogata H., Pesant S., Raes J., Sieracki M. E., Speich S., Stemmann L., Sunagawa S., Weissenbach J., Wincker P., Karsenti E., Boss E., Follows M., Karp-Boss L., Krzic U., Reynaud E. G., Sardet C., Sullivan M. B., Velayoudon D., Ocean plankton. Eukaryotic plankton diversity in the sunlit ocean. Science 348, 1261605 (2015). PubMed

Strzepek R. F., Nunn B. L., Bach L. T., Berges J. A., Young E. B., Boyd P. W., The ongoing need for rates: Can physiology and omics come together to co-design the measurements needed to understand complex ocean biogeochemistry? J. Plankton Res. 44, 485–495 (2022). PubMed PMC

Zuñiga C., Li C.-T., Yu G., Al-Bassam M. M., Li T., Jiang L., Zaramela L. S., Guarnieri M., Betenbaugh M. J., Zengler K., Environmental stimuli drive a transition from cooperation to competition in synthetic phototrophic communities. Nat. Microbiol. 4, 2184–2191 (2019). PubMed

Wang H., Marcišauskas S., Sánchez B. J., Domenzain I., Hermansson D., Agren R., Nielsen J., Kerkhoven E. J., RAVEN 2.0: A versatile toolbox for metabolic network reconstruction and a case study on Streptomyces coelicolor. PLOS Comput. Biol. 14, e1006541 (2018). PubMed PMC

Ebrahim A., Lerman J. A., Palsson B. O., Hyduke D. R., COBRApy: COnstraints-based reconstruction and analysis for Python. BMC Syst. Biol. 7, 74 (2013). PubMed PMC

Heirendt L., Arreckx S., Pfau T., Mendoza S. N., Richelle A., Heinken A., Haraldsdóttir H. S., Wachowiak J., Keating S. M., Vlasov V., Magnusdóttir S., Ng C. Y., Preciat G., Žagare A., Chan S. H. J., Aurich M. K., Clancy C. M., Modamio J., Sauls J. T., Noronha A., Bordbar A., Cousins B., El Assal D. C., Valcarcel L. V., Apaolaza I., Ghaderi S., Ahookhosh M., Ben Guebila M., Kostromins A., Sompairac N., Le H. M., Ma D., Sun Y., Wang L., Yurkovich J. T., Oliveira M. A. P., Vuong P. T., El Assal L. P., Kuperstein I., Zinovyev A., Hinton H. S., Bryant W. A., Aragón Artacho F. J., Planes F. J., Stalidzans E., Maass A., Vempala S., Hucka M., Saunders M. A., Maranas C. D., Lewis N. E., Sauter T., Palsson B. Ø., Thiele I., Fleming R. M. T., Creation and analysis of biochemical constraint-based models using the COBRA Toolbox v.3.0. Nat. Protoc. 14, 639–702 (2019). PubMed PMC

Chang R. L., Ghamsari L., Manichaikul A., Hom E. F. Y., Balaji S., Fu W., Shen Y., Hao T., Palsson B. Ø., Salehi-Ashtiani K., Papin J. A., Metabolic network reconstruction of Chlamydomonas offers insight into light-driven algal metabolism. Mol. Syst. Biol. 7, 518 (2011). PubMed PMC

King Z. A., Lu J., Dräger A., Miller P., Federowicz S., Lerman J. A., Ebrahim A., Palsson B. O., Lewis N. E., BiGG models: A platform for integrating, standardizing and sharing genome-scale models. Nucleic Acids Res. 44, D515–D522 (2016). PubMed PMC

Moretti S., Tran V. D. T., Mehl F., Ibberson M., Pagni M., MetaNetX/MNXref: Unified namespace for metabolites and biochemical reactions in the context of metabolic models. Nucleic Acids Res. 49, D570–D574 (2021). PubMed PMC

Elagoz A. M., Ambrosino L., Lauritano C., De novo transcriptome of the diatom Cylindrotheca closterium identifies genes involved in the metabolism of anti-inflammatory compounds. Sci. Rep. 10, 4138 (2020). PubMed PMC

Megchelenbrink W., Huynen M., Marchiori E., optGpSampler: An improved tool for uniformly sampling the solution-space of genome-scale metabolic networks. PLOS ONE 9, e86587 (2014). PubMed PMC

Sunagawa S., Acinas S. G., Bork P., Bowler C., Acinas S. G., Babin M., Bork P., Boss E., Bowler C., Cochrane G., de Vargas C., Follows M., Gorsky G., Grimsley N., Guidi L., Hingamp P., Iudicone D., Jaillon O., Kandels S., Karp-Boss L., Karsenti E., Lescot M., Not F., Ogata H., Pesant S., Poulton N., Raes J., Sardet C., Sieracki M., Speich S., Stemmann L., Sullivan M. B., Sunagawa S., Wincker P., Eveillard D., Gorsky G., Guidi L., Iudicone D., Karsenti E., Lombard F., Ogata H., Pesant S., Sullivan M. B., Wincker P., de Vargas C., Tara Oceans: Towards global ocean ecosystems biology. Nat. Rev. Microbiol. 18, 428–445 (2020). PubMed

Jensen E. L., Yangüez K., Carrière F., Gontero B., Storage compound accumulation in diatoms as response to elevated CO2 concentration. Biology 9, 5 (2019). PubMed PMC

Wu S., Gu W., Jia S., Wang L., Wang L., Liu X., Zhou L., Huang A., Wang G., Proteomic and biochemical responses to different concentrations of CO2 suggest the existence of multiple carbon metabolism strategies in Phaeodactylum tricornutum. Biotechnol. Biofuels 14, 235 (2021). PubMed PMC

Nakajima K., Tanaka A., Matsuda Y., SLC4 family transporters in a marine diatom directly pump bicarbonate from seawater. Proc. Natl. Acad. Sci. U.S.A 110, 1767–1772 (2013). PubMed PMC

Yodsuwan N., Sawayama S., Sirisansaneeyakul S., Effect of nitrogen concentration on growth, lipid production and fatty acid profiles of the marine diatom Phaeodactylum tricornutum. Agric. Nat. Resour. 51, 190–197 (2017).

Yang Z.-K., Ma Y.-H., Zheng J.-W., Yang W.-D., Liu J.-S., Li H.-Y., Proteomics to reveal metabolic network shifts towards lipid accumulation following nitrogen deprivation in the diatom Phaeodactylum tricornutum. J. Appl. Phycol. 26, 73–82 (2014). PubMed PMC

Zhang Y., Wu H., Sun M., Peng Q., Li A., Photosynthetic physiological performance and proteomic profiling of the oleaginous algae Scenedesmus acuminatus reveal the mechanism of lipid accumulation under low and high nitrogen supplies. Photosynth. Res. 138, 73–102 (2018). PubMed

Hockin N. L., Mock T., Mulholland F., Kopriva S., Malin G., The response of diatom central carbon metabolism to nitrogen starvation is different from that of green algae and higher plants. Plant Physiol. 158, 299–312 (2012). PubMed PMC

Jian J., Zeng D., Wei W., Lin H., Li P., Liu W., The combination of RNA and protein profiling reveals the response to nitrogen depletion in Thalassiosira pseudonana. Sci. Rep. 7, 8989 (2017). PubMed PMC

Msanne J., Xu D., Konda A. R., Casas-Mollano J. A., Awada T., Cahoon E. B., Cerutti H., 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 (2012). PubMed

Recht L., Zarka A., Boussiba S., Patterns of carbohydrate and fatty acid changes under nitrogen starvation in the microalgae Haematococcus pluvialis and Nannochloropsis sp. Appl. Microbiol. Biotechnol. 94, 1495–1503 (2012). PubMed

Dean A. P., Sigee D. C., Estrada B., Pittman J. K., Using FTIR spectroscopy for rapid determination of lipid accumulation in response to nitrogen limitation in freshwater microalgae. Bioresour. Technol. 101, 4499–4507 (2010). PubMed

Qari H. A., Oves M., Fatty acid synthesis by Chlamydomonas reinhardtii in phosphorus limitation. J. Bioenerg. Biomembr. 52, 27–38 (2020). PubMed

Chen M., Li J., Dai X., Sun Y., Chen F., Effect of phosphorus and temperature on chlorophyll a contents and cell sizes of Scenedesmus obliquus and Microcystis aeruginosa. Limnology 12, 187–192 (2011).

Zhou B., Ma J., Chen F., Zou Y., Wei Y., Zhong H., Pan K., Mechanisms underlying silicon-dependent metal tolerance in the marine diatom Phaeodactylum tricornutum. Environ. Pollut. 262, 114331 (2020). PubMed

Cheng J., Feng J., Sun J., Huang Y., Zhou J., Cen K., Enhancing the lipid content of the diatom Nitzschia sp. by 60 Co-γ irradiation mutation and high-salinity domestication. Energy 78, 9–15 (2014).

d’Ippolito G., Sardo A., Paris D., Vella F. M., Adelfi M. G., Botte P., Gallo C., Fontana A., Potential of lipid metabolism in marine diatoms for biofuel production. Biotechnol. Biofuels 8, 28 (2015). PubMed PMC

Armstrong E., Rogerson A., Leftley J. W., The abundance of heterotrophic protists associated with intertidal seaweeds. Estuar. Coast. Shelf Sci. 50, 415–424 (2000).

Villanova V., Spetea C., Mixotrophy in diatoms: Molecular mechanism and industrial potential. Physiol. Plant. 173, 603–611 (2021). PubMed

Bailleul B., Berne N., Murik O., Petroutsos D., Prihoda J., Tanaka A., Villanova V., Bligny R., Flori S., Falconet D., Krieger-Liszkay A., Santabarbara S., Rappaport F., Joliot P., Tirichine L., Falkowski P. G., Cardol P., Bowler C., Finazzi G., Energetic coupling between plastids and mitochondria drives CO2 assimilation in diatoms. Nature 524, 366–369 (2015). PubMed

Stoecker D. K., Hansen P. J., Caron D. A., Mitra A., Mixotrophy in the marine plankton. Ann. Rev. Mar. Sci. 9, 311–335 (2017). PubMed

Meyer N., Rydzyk A., Pohnert G., Pronounced uptake and metabolism of organic substrates by diatoms revealed by pulse-labeling metabolomics. Front. Mar. Sci. 9, 821167 (2022).

Caron D. A., Mixotrophy stirs up our understanding of marine food webs. Proc. Natl. Acad. Sci. U.S.A. 113, 2806–2808 (2016). PubMed PMC

Amin S. A., Parker M. S., Armbrust E. V., Interactions between diatoms and bacteria. Microbiol. Mol. Biol. Rev. 76, 667–684 (2012). PubMed PMC

Liu J., Xue C.-X., Sun H., Zheng Y., Meng Z., Zhang X.-H., Carbohydrate catabolic capability of a Flavobacteriia bacterium isolated from hadal water. Syst. Appl. Microbiol. 42, 263–274 (2019). PubMed

Kallscheuer N., Wiegand S., Kohn T., Boedeker C., Jeske O., Rast P., Müller R.-W., Brümmer F., Heuer A., Jetten M. S. M., Rohde M., Jogler M., Jogler C., Cultivation-independent analysis of the bacterial community associated with the calcareous sponge Clathrina clathrus and isolation of Poriferisphaera corsica Gen. Nov., Sp. Nov., belonging to the barely studied class Phycisphaerae in the Phylum Planctomycetes. Front. Microbiol. 11, 602250 (2020). PubMed PMC

Fukunaga Y., Kurahashi M., Sakiyama Y., Ohuchi M., Yokota A., Harayama S., Phycisphaera mikurensis gen. nov., sp. nov., isolated from a marine alga, and proposal of Phycisphaeraceae fam. nov., Phycisphaerales ord. nov. and Phycisphaerae classis nov. in the phylum Planctomycetes. J. Gen. Appl. Microbiol. 55, 267–275 (2009). PubMed

Priest T., Heins A., Harder J., Amann R., Fuchs B. M., Niche partitioning of the ubiquitous and ecologically relevant NS5 marine group. ISME J. 16, 1570–1582 (2022). PubMed PMC

Buchan A., LeCleir G. R., Gulvik C. A., González J. M., Master recyclers: Features and functions of bacteria associated with phytoplankton blooms. Nat. Rev. Microbiol. 12, 686–698 (2014). PubMed

Thiele I., Palsson B. Ø., A protocol for generating a high-quality genome-scale metabolic reconstruction. Nat. Protoc. 5, 93–121 (2010). PubMed PMC

M. Kumar, C. Zuniga, J. D. Tibocha-Bonilla, S. R. Smith, J. Coker, A. E. Allen, K. Zengler, “Constraint-based modeling of diatoms metabolism and quantitative biology approaches” in The Molecular Life of Diatoms (Springer International Publishing, 2022; https://link.springer.com/10.1007/978-3-030-92499-7_26), pp. 775–808. DOI

Stock W., Vanelslander B., Rüdiger F., Sabbe K., Vyverman W., Karsten U., Thermal niche differentiation in the benthic diatom Cylindrotheca closterium (Bacillariophyceae) complex. Front. Microbiol. 10, 1395 (2019). PubMed PMC

Hutchins D. A., Fu F., Microorganisms and ocean global change. Nat. Microbiol. 2, 17058 (2017). PubMed

Pahl S. L., Lewis D. M., Chen F., King K. D., Growth dynamics and the proximate biochemical composition and fatty acid profile of the heterotrophically grown diatom Cyclotella cryptica. J. Appl. Phycol. 22, 165–171 (2010). PubMed PMC

Armstrong E., Rogerson A., Leftley J. W., Utilisation of seaweed carbon by three surface-associated heterotrophic protists, Stereomyxa ramosa, Nitzschia alba and Labyrinthula sp. Aquat. Microb. Ecol. 21, 49–57 (2000).

Brzezinski M. A., The Si:C:N ratio of marine diatoms: Interspecific variability and the effect of some environmental variables. J. Phycol. 21, 347–357 (2004).

Lachance J.-C., Lloyd C. J., Monk J. M., Yang L., Sastry A. V., Seif Y., Palsson B. O., Rodrigue S., Feist A. M., King Z. A., Jacques P.-É., BOFdat: Generating biomass objective functions for genome-scale metabolic models from experimental data. PLOS Comput. Biol. 15, e1006971 (2019). PubMed PMC

Jallet D., Caballero M. A., Gallina A. A., Youngblood M., Peers G., Photosynthetic physiology and biomass partitioning in the model diatom Phaeodactylum tricornutum grown in a sinusoidal light regime. Algal Res. 18, 51–60 (2016).

Cunha E., Lagoa D., Faria J. P., Liu F., Henry C. S., Dias O., TranSyT, an innovative framework for identifying transport systems. Bioinformatics 39, btad466 (2023). PubMed PMC

Lieven C., Beber M. E., Olivier B. G., Bergmann F. T., Ataman M., Babaei P., Bartell J. A., Blank L. M., Chauhan S., Correia K., Diener C., Dräger A., Ebert B. E., Edirisinghe J. N., Faria J. P., Feist A. M., Fengos G., Fleming R. M. T., García-Jiménez B., Hatzimanikatis V., van Helvoirt W., Henry C. S., Hermjakob H., Herrgård M. J., Kaafarani A., Kim H. U., King Z., Klamt S., Klipp E., Koehorst J. J., König M., Lakshmanan M., Lee D.-Y., Lee S. Y., Lee S., Lewis N. E., Liu F., Ma H., Machado D., Mahadevan R., Maia P., Mardinoglu A., Medlock G. L., Monk J. M., Nielsen J., Nielsen L. K., Nogales J., Nookaew I., Palsson B. O., Papin J. A., Patil K. R., Poolman M., Price N. D., Resendis-Antonio O., Richelle A., Rocha I., Sánchez B. J., Schaap P. J., Sheriff R. S. M., Shoaie S., Sonnenschein N., Teusink B., Vilaça P., Vik J. O., Wodke J. A. H., Xavier J. C., Yuan Q., Zakhartsev M., Zhang C., MEMOTE for standardized genome-scale metabolic model testing. Nat. Biotechnol. 38, 272–276 (2020). PubMed PMC

Orth J. D., Thiele I., Palsson B. Ø., What is flux balance analysis? Nat. Biotechnol. 28, 245–248 (2010). PubMed PMC

Morel F. M. M., Rueter J. G., Anderson D. M., Guillard R. R. L., AQUIL: A chemically defined phytoplankton culture medium for trace metal studies. J. Phycol. 15, 135–141 (1979).

Kim D., Langmead B., Salzberg S. L., HISAT: A fast spliced aligner with low memory requirements. Nat. Methods 12, 357–360 (2015). PubMed PMC

Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R., The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009). PubMed PMC

Caballero J., Smit A. F. A., Hood L., Glusman G., Realistic artificial DNA sequences as negative controls for computational genomics. Nucleic Acids Res. 42, e99–e99 (2014). PubMed PMC

Quinlan A. R., Hall I. M., BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010). PubMed PMC

B. G. Galuzzi, L. Milazzo, C. Damiani, Best Practices in Flux Sampling of Constrained-Based Models (Springer, 2023; 10.1007/978-3-031-25891-6_18), pp. 234–248. DOI

Segata N., Izard J., Waldron L., Gevers D., Miropolsky L., Garrett W. S., Huttenhower C., Metagenomic biomarker discovery and explanation. Genome Biol. 12, R60 (2011). PubMed PMC

Monk J., Nogales J., Palsson B. O., Optimizing genome-scale network reconstructions. Nat. Biotechnol. 32, 447–452 (2014). PubMed

Morris E. P., Kromkamp J. C., Influence of temperature on the relationship between oxygen- and fluorescence-based estimates of photosynthetic parameters in a marine benthic diatom (Cylindrotheca closterium). Eur. J. Phycol. 38, 133–142 (2003).

Alcoverro T., Conte E., Mazzella L., Production of mucilage by the adriatic epipelic diatom Cylindrotheca closterium (Bacillariophyceae) under nutrient limitation. J. Phycol. 36, 1087–1095 (2000).

Rijstenbil J. W., Effects of UVB radiation and salt stress on growth, pigments and antioxidative defence of the marine diatom Cylindrotheca closterium. Mar. Ecol. Prog. Ser. 254, 37–48 (2003).

Rijstenbil J. W., UV- and salinity-induced oxidative effects in the marine diatom Cylindrotheca closterium during simulated emersion. Mar. Biol. 147, 1063–1073 (2005).

Staats N., Stal L. J., Mur L. R., Exopolysaccharide production by the epipelic diatom Cylindrotheca closterium: Effects of nutrient conditions. J. Exp. Mar. Bio. Ecol. 249, 13–27 (2000). PubMed

Wang S., Sirbu D., Thomsen L., Kuhnert N., Ullrich M. S., Thomsen C., Comparative lipidomic studies of Scenedesmus sp. (Chlorophyceae) and Cylindrotheca closterium (Bacillariophyceae) reveal their differences in lipid production under nitrogen starvation. J. Phycol. 55, 1246–1257 (2019). PubMed

Araújo C. V. M., Diz F. R., Lubián L. M., Blasco J., Moreno-Garrido I., Sensitivity of Cylindrotheca closterium to copper: Influence of three test endpoints and two test methods. Sci. Total Environ. 408, 3696–3703 (2010). PubMed

Almeyda M. D., Scodelaro Bilbao P. G., Popovich C. A., Constenla D., Leonardi P. I., Enhancement of polyunsaturated fatty acid production under low-temperature stress in Cylindrotheca closterium. J. Appl. Phycol. 32, 989–1001 (2020).

Van Bergeijk S. A., Van der Zee C., Stal L. J., Uptake and excretion of dimethylsulphoniopropionate is driven by salinity changes in the marine benthic diatom Cylindrotheca closterium. Eur. J. Phycol. 38, 341–349 (2003).

Erdogan A., Demirel Z., Dalay M. C., Eroglu A. E., Fucoxanthin content of Cylindrotheca closterium and its oxidative stress mediated enhancement. Turkish J. Fish. Aquat. Sci. 16, 499–506 (2016).

Orcutt D. M., Patterson G. W., Effect of light intensity upon lipid composition of Nitzschia closterium (Cylindrotheca fusiformis). Lipids 9, 1000–1003 (1974). PubMed

Affan A., Heo S., Jeon Y., Lee J., Optimal growth conditions and antioxidative activities of Cylindrotheca closterium (Bacillariophyceae). J. Phycol. 45, 1405–1415 (2009). PubMed

Brembu T., Mühlroth A., Alipanah L., Bones A. M., The effects of phosphorus limitation on carbon metabolism in diatoms. Philos. Trans. R. Soc. B Biol. Sci. 372, 20160406 (2017). PubMed PMC

Ruocco N., Nuzzo G., D’Ippolito G., Manzo E., Sardo A., Ianora A., Romano G., Iuliano A., Zupo V., Costantini M., Fontana A., Lipoxygenase pathways in diatoms: Occurrence and correlation with grazer toxicity in four benthic species. Mar. Drugs 18, 66 (2020). PubMed PMC

Ryabushko V. I., Zheleznova S. N., Nekhoroshev M. V., Effect of nitrogen on fucoxanthin accumulation in the diatom Cylindrotheca closterium (Ehrenb.) Reimann et Lewin. Int. J. Algae 19, 79–84 (2017).

Han T., Song P., Shi R., Qi Z., Li J., Huang H., Optimal nutrient availability could alleviate diatom Cylindrotheca closterium fouling during seedling cultivation of Sargassum hemiphyllum. Aquaculture 552, 738020 (2022).

Becker A. E., Copplestone D., Cadmium uptake from sediment by Cylindrotheca closterium and the effect of diatom presence on partitioning of cadmium between sediment and water: A laboratory study. Limnol. Oceanogr. 64, 2550–2568 (2019).

Humphrey G., Subba Rao D., Photosynthetic rate of the marine diatom Cylindrotheca closterium. Mar. Freshw. Res. 18, 123 (1967).

Zhang F., Chi J., Influences of nutritional conditions on degradation of dibutyl phthalate in coastal sediments with Cylindrotheca closterium. Mar. Pollut. Bull. 153, 111021 (2020). PubMed

Roncarati F., Rijstenbil J. W., Pistocchi R., Photosynthetic performance, oxidative damage and antioxidants in Cylindrotheca closterium in response to high irradiance, UVB radiation and salinity. Mar. Biol. 153, 965–973 (2008).

Wolfstein K., de Brouwer J., Stal L., Biochemical partitioning of photosynthetically fixed carbon by benthic diatoms during short-term incubations at different irradiances. Mar. Ecol. Prog. Ser. 245, 21–31 (2002).

Wolfstein K., Stal L., Production of extracellular polymeric substances (EPS) by benthic diatoms: Effect of irradiance and temperature. Mar. Ecol. Prog. Ser. 236, 13–22 (2002).

Suman K., Kiran T., Devi U. K., Sarma N. S., Culture medium optimization and lipid profiling of Cylindrotheca, a lipid- and polyunsaturated fatty acid-rich pennate diatom and potential source of eicosapentaenoic acid. Bot. Mar. 55, 289–299 (2012).

Underwood G. J. C., Boulcott M., Raines C. A., Waldron K., Environmental effects on exopolymer production by marine benthic diatoms: Dynamics, changes in composition, and pathways of production. J. Phycol. 40, 293–304 (2004).

Admiraal W., Laane R., Peletier H., Participation of diatoms in the amino acid cycle of coastal waters; uptake and excretion in cultures. Mar. Ecol. Prog. Ser. 15, 303–306 (1984).

De Brouwer J. F. C., Stal L. J., Daily fluctuations of exopolymers in cultures of the benthic diatoms Cylindrotheca closterium and Nitzschia sp. (Bacillariophyceae). J. Phycol. 38, 464–472 (2002).

Zheleznova S. N., Production characteristics of the diatom Cylindrotheca closterium (Ehrenb.) Reimann et Lewin grown in an intensive culture at various nitrogen sources in the medium. Mar. Biol. J. 4, 33–44 (2019).

Nilsson C., Sundback K., Sundback K., Amino acid uptake in natural microphytobenthic assemblages studied by microautoradiography. Hydrobiologia 332, 119–129 (1996).

Staats N., De Winder B., Mur L. R., Stal L. J., Isolation and characterization of extracellular polysaccharides from the epipelic diatoms Cylindrotheca closterium and Navicula salinarum. Eur. J. Phycol. 34, 161–169 (1999).

Urbani R., Magaletti E., Sist P., Cicero A. M., Extracellular carbohydrates released by the marine diatoms Cylindrotheca closterium, Thalassiosira pseudonana and Skeletonema costatum: Effect of P-depletion and growth status. Sci. Total Environ. 353, 300–306 (2005). PubMed

Wolf Y. I., Koonin E. V., A tight link between orthologs and bidirectional best hits in bacterial and archaeal genomes. Genome Biol. Evol. 4, 1286–1294 (2012). PubMed PMC

Kanehisa M., Sato Y., Kawashima M., KEGG mapping tools for uncovering hidden features in biological data. Protein Sci. 31, 47–53 (2022). PubMed PMC

Seaver S. M. D., Liu F., Zhang Q., Jeffryes J., Faria J. P., Edirisinghe J. N., Mundy M., Chia N., Noor E., Beber M. E., Best A. A., DeJongh M., Kimbrel J. A., D’haeseleer P., McCorkle S. R., Bolton J. R., Pearson E., Canon S., Wood-Charlson E. M., Cottingham R. W., Arkin A. P., Henry C. S., The ModelSEED Biochemistry Database for the integration of metabolic annotations and the reconstruction, comparison and analysis of metabolic models for plants, fungi and microbes. Nucleic Acids Res. 49, D575–D588 (2021). PubMed PMC

Caspi R., Billington R., Keseler I. M., Kothari A., Krummenacker M., Midford P. E., Ong W. K., Paley S., Subhraveti P., Karp P. D., The MetaCyc database of metabolic pathways and enzymes - A 2019 update. Nucleic Acids Res. 48, D445–D453 (2020). PubMed PMC

Bateman A., Martin M.-J., Orchard S., Magrane M., Agivetova R., Ahmad S., Alpi E., Bowler-Barnett E. H., Britto R., Bursteinas B., Bye-A-Jee H., Coetzee R., Cukura A., Da Silva A., Denny P., Dogan T., Ebenezer T., Fan J., Castro L. G., Garmiri P., Georghiou G., Gonzales L., Hatton-Ellis E., Hussein A., Ignatchenko A., Insana G., Ishtiaq R., Jokinen P., Joshi V., Jyothi D., Lock A., Lopez R., Luciani A., Luo J., Lussi Y., MacDougall A., Madeira F., Mahmoudy M., Menchi M., Mishra A., Moulang K., Nightingale A., Oliveira C. S., Pundir S., Qi G., Raj S., Rice D., Lopez M. R., Saidi R., Sampson J., Sawford T., Speretta E., Turner E., Tyagi N., Vasudev P., Volynkin V., Warner K., Watkins X., Zaru R., Zellner H., Bridge A., Poux S., Redaschi N., Aimo L., Argoud-Puy G., Auchincloss A., Axelsen K., Bansal P., Baratin D., Blatter M.-C., Bolleman J., Boutet E., Breuza L., Casals-Casas C., de Castro E., Echioukh K. C., Coudert E., Cuche B., Doche M., Dornevil D., Estreicher A., Famiglietti M. L., Feuermann M., Gasteiger E., Gehant S., Gerritsen V., Gos A., Gruaz-Gumowski N., Hinz U., Hulo C., Hyka-Nouspikel N., Jungo F., Keller G., Kerhornou A., Lara V., Le Mercier P., Lieberherr D., Lombardot T., Martin X., Masson P., Morgat A., Neto T. B., Paesano S., Pedruzzi I., Pilbout S., Pourcel L., Pozzato M., Pruess M., Rivoire C., Sigrist C., Sonesson K., Stutz A., Sundaram S., Tognolli M., Verbregue L., Wu C. H., Arighi C. N., Arminski L., Chen C., Chen Y., Garavelli J. S., Huang H., Laiho K., McGarvey P., Natale D. A., Ross K., Vinayaka C. R., Wang Q., Wang Y., Yeh L.-S., Zhang J., Ruch P., Teodoro D., UniProt: The universal protein knowledgebase in 2021. Nucleic Acids Res. 49, D480–D489 (2021). PubMed PMC

Chang A., Jeske L., Ulbrich S., Hofmann J., Koblitz J., Schomburg I., Neumann-Schaal M., Jahn D., Schomburg D., BRENDA, the ELIXIR core data resource in 2021: New developments and updates. Nucleic Acids Res. 49, D498–D508 (2021). PubMed PMC

Fleischmann A., IntEnz, the integrated relational enzyme database. Nucleic Acids Res. 32, 434D–4437D (2004). PubMed PMC

Saier M. H., Reddy V. S., Moreno-Hagelsieb G., Hendargo K. J., Zhang Y., Iddamsetty V., Lam K. J. K., Tian N., Russum S., Wang J., Medrano-Soto A., The Transporter Classification Database (TCDB): 2021 update. Nucleic Acids Res. 49, D461–D467 (2021). PubMed PMC

Elbourne L. D. H., Tetu S. G., Hassan K. A., Paulsen I. T., TransportDB 2.0: A database for exploring membrane transporters in sequenced genomes from all domains of life. Nucleic Acids Res. 45, D320–D324 (2017). PubMed PMC

Petersen T. N., Brunak S., von Heijne G., Nielsen H., SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785–786 (2011). PubMed

Gschloessl B., Guermeur Y., Cock J. M., HECTAR: A method to predict subcellular targeting in heterokonts. BMC Bioinformatics 9, 393 (2008). PubMed PMC

Claros M. G., MitoProt, a Macintosh application for studying mitochondrial proteins. Bioinformatics 11, 441–447 (1995). PubMed

Cokol M., Nair R., Rost B., Finding nuclear localization signals. EMBO Rep. 1, 411–415 (2000). PubMed PMC

Emanuelsson O., Brunak S., von Heijne G., Nielsen H., Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2, 953–971 (2007). PubMed

Grant B., Madgwick J., Dal P. G., Growth of Cylindrotheca closterium var. californica (Mereschk.) Reimann & Lewin on nitrate, ammonia, and urea. Mar. Freshw. Res. 18, 129 (1967).

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...