Proteomic study uncovers molecular principles of single-cell-level phenotypic heterogeneity in lipid storage of Nannochloropsis oceanica View Full Text


Ontology type: schema:ScholarlyArticle      Open Access: True


Article Info

DATE

2019-12

AUTHORS

Chaoyun Chen, Andreas Harst, Wuxin You, Jian Xu, Kang Ning, Ansgar Poetsch

ABSTRACT

Background: Nannochloropsis oceanica belongs to a large group of photoautotrophic eukaryotic organisms that play important roles in fixation and cycling of atmospheric CO2. Its capability of storing solar energy and carbon dioxide in the form of triacylglycerol (TAG) of up to 60% of total weight under nitrogen deprivation stress sparked interest in its use for biofuel production. Phenotypes varying in lipid accumulation among an N. oceanica population can be disclosed by single-cell analysis/sorting using fluorescence-activated cell sorting (FACS); yet the phenomenon of single cell heterogeneity in an algae population remains to be fully understood at the molecular level. In this study, combination of FACS and proteomics was used for identification, quantification and differentiation of these heterogeneities on the molecular level. Results: For N. oceanica cultivated under nitrogen deplete (-N) and replete (+N) conditions, two groups differing in lipid content were distinguished. These differentiations could be recognized on the population as well as the single-cell levels; proteomics uncovered alterations in carbon fixation and flux, photosynthetic machinery, lipid storage and turnover in the populations. Although heterogeneity patterns have been affected by nitrogen supply and cultivation conditions of the N. oceanica populations, differentiation itself seems to be very robust against these factors: cultivation under +N, -N, in shaker bottles, and in a photo-bioreactor all split into two subpopulations. Intriguingly, population heterogeneity resumed after subpopulations were separately recultivated for a second round, refuting the possible development of genetic heterogeneity in the course of sorting and cultivation. Conclusions: This work illustrates for the first time the feasibility of combining FACS and (prote)-omics for mechanistic understanding of phenotypic heterogeneity in lipid-producing microalgae. Such combinatorial method can facilitate molecular breeding and design of bioprocesses. More... »

PAGES

21

References to SciGraph publications

  • 2016-10. Probing the metabolic heterogeneity of live Euglena gracilis with stimulated Raman scattering microscopy in NATURE MICROBIOLOGY
  • 2011-10. Improved Nile Red staining of Nannochloropsis sp. in JOURNAL OF APPLIED PHYCOLOGY
  • 2008-12. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification in NATURE BIOTECHNOLOGY
  • 2015-12. The use of fluorescent Nile red and BODIPY for lipid measurement in microalgae in BIOTECHNOLOGY FOR BIOFUELS
  • 2010-09-17. The role of physiological heterogeneity in microbial population behavior in NATURE CHEMICAL BIOLOGY
  • 2017-12. Label-free, simultaneous quantification of starch, protein and triacylglycerol in single microalgal cells in BIOTECHNOLOGY FOR BIOFUELS
  • 2010-09. Advanced tool for characterization of microbial cultures by combining cytomics and proteomics in APPLIED MICROBIOLOGY AND BIOTECHNOLOGY
  • 2017-01-23. MetaSort untangles metagenome assembly by reducing microbial community complexity in NATURE COMMUNICATIONS
  • 1998-08. Self-organization, complexity and chaos: The new biology for medicine in NATURE MEDICINE
  • 2012-10. Quick estimation of intraspecific variation of fatty acid composition in Dunaliella salina using flow cytometry and Nile Red in JOURNAL OF APPLIED PHYCOLOGY
  • 1975. Culture of Phytoplankton for Feeding Marine Invertebrates in CULTURE OF MARINE INVERTEBRATE ANIMALS
  • 2014-12. Quantitative dynamics of triacylglycerol accumulation in microalgae populations at single-cell resolution revealed by Raman microspectroscopy in BIOTECHNOLOGY FOR BIOFUELS
  • Identifiers

    URI

    http://scigraph.springernature.com/pub.10.1186/s13068-019-1361-7

    DOI

    http://dx.doi.org/10.1186/s13068-019-1361-7

    DIMENSIONS

    https://app.dimensions.ai/details/publication/pub.1111909569

    PUBMED

    https://www.ncbi.nlm.nih.gov/pubmed/30740142


    Indexing Status Check whether this publication has been indexed by Scopus and Web Of Science using the SN Indexing Status Tool
    Incoming Citations Browse incoming citations for this publication using opencitations.net

    JSON-LD is the canonical representation for SciGraph data.

    TIP: You can open this SciGraph record using an external JSON-LD service: JSON-LD Playground Google SDTT

    [
      {
        "@context": "https://springernature.github.io/scigraph/jsonld/sgcontext.json", 
        "about": [
          {
            "id": "http://purl.org/au-research/vocabulary/anzsrc-for/2008/0601", 
            "inDefinedTermSet": "http://purl.org/au-research/vocabulary/anzsrc-for/2008/", 
            "name": "Biochemistry and Cell Biology", 
            "type": "DefinedTerm"
          }, 
          {
            "id": "http://purl.org/au-research/vocabulary/anzsrc-for/2008/06", 
            "inDefinedTermSet": "http://purl.org/au-research/vocabulary/anzsrc-for/2008/", 
            "name": "Biological Sciences", 
            "type": "DefinedTerm"
          }
        ], 
        "author": [
          {
            "affiliation": {
              "alternateName": "Huazhong University of Science and Technology", 
              "id": "https://www.grid.ac/institutes/grid.33199.31", 
              "name": [
                "Key Laboratory of Molecular Biophysics of the Ministry of Education, Hubei Key Laboratory of Bioinformatics and Molecular-imaging, Department of Bioinformatics and Systems Biology, College of Life Science and Technology, Huazhong University of Science and Technology, 430074, Wuhan, Hubei, China"
              ], 
              "type": "Organization"
            }, 
            "familyName": "Chen", 
            "givenName": "Chaoyun", 
            "type": "Person"
          }, 
          {
            "affiliation": {
              "alternateName": "Ruhr University Bochum", 
              "id": "https://www.grid.ac/institutes/grid.5570.7", 
              "name": [
                "Plant Biochemistry, Ruhr University Bochum, 44801, Bochum, Germany"
              ], 
              "type": "Organization"
            }, 
            "familyName": "Harst", 
            "givenName": "Andreas", 
            "type": "Person"
          }, 
          {
            "affiliation": {
              "alternateName": "Qingdao Institute of Bioenergy and Bioprocess Technology", 
              "id": "https://www.grid.ac/institutes/grid.458500.c", 
              "name": [
                "Plant Biochemistry, Ruhr University Bochum, 44801, Bochum, Germany", 
                "Single-Cell Center, CAS Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, 266101, Qingdao, Shandong, China"
              ], 
              "type": "Organization"
            }, 
            "familyName": "You", 
            "givenName": "Wuxin", 
            "type": "Person"
          }, 
          {
            "affiliation": {
              "alternateName": "Qingdao Institute of Bioenergy and Bioprocess Technology", 
              "id": "https://www.grid.ac/institutes/grid.458500.c", 
              "name": [
                "Single-Cell Center, CAS Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, 266101, Qingdao, Shandong, China"
              ], 
              "type": "Organization"
            }, 
            "familyName": "Xu", 
            "givenName": "Jian", 
            "type": "Person"
          }, 
          {
            "affiliation": {
              "alternateName": "Huazhong University of Science and Technology", 
              "id": "https://www.grid.ac/institutes/grid.33199.31", 
              "name": [
                "Key Laboratory of Molecular Biophysics of the Ministry of Education, Hubei Key Laboratory of Bioinformatics and Molecular-imaging, Department of Bioinformatics and Systems Biology, College of Life Science and Technology, Huazhong University of Science and Technology, 430074, Wuhan, Hubei, China"
              ], 
              "type": "Organization"
            }, 
            "familyName": "Ning", 
            "givenName": "Kang", 
            "type": "Person"
          }, 
          {
            "affiliation": {
              "alternateName": "Plymouth University", 
              "id": "https://www.grid.ac/institutes/grid.11201.33", 
              "name": [
                "Plant Biochemistry, Ruhr University Bochum, 44801, Bochum, Germany", 
                "School of Biomedical and Healthcare Sciences, Plymouth University, PL4 8AA, Plymouth, UK"
              ], 
              "type": "Organization"
            }, 
            "familyName": "Poetsch", 
            "givenName": "Ansgar", 
            "type": "Person"
          }
        ], 
        "citation": [
          {
            "id": "https://doi.org/10.1371/journal.pone.0085731", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1000154881"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.mimet.2006.07.005", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1001020024"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nchembio.436", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1003940702", 
              "https://doi.org/10.1038/nchembio.436"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1371/journal.pone.0160711", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1006327278"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.ymben.2015.06.008", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1006710224"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.ymben.2015.06.008", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1006710224"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.ymben.2015.06.008", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1006710224"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.ymben.2015.06.008", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1006710224"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.biortech.2014.01.017", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1007821347"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1111/nph.13728", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1010046819"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/1754-6834-7-58", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1010497314", 
              "https://doi.org/10.1186/1754-6834-7-58"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nmicrobiol.2016.124", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1011179589", 
              "https://doi.org/10.1038/nmicrobiol.2016.124"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1037/1082-989x.10.1.21", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1015425693"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1128/jb.00310-08", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1016525614"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1111/nph.13843", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1017663686"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1073/pnas.1610758113", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1017987367"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1074/mcp.m113.031591", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1019972763"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1002/cyto.a.20683", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1020721335"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/nar/gkw880", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1022739704"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1007/s10811-011-9768-y", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1023799797", 
              "https://doi.org/10.1007/s10811-011-9768-y"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/s13068-015-0220-4", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1025480930", 
              "https://doi.org/10.1186/s13068-015-0220-4"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/s13068-015-0220-4", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1025480930", 
              "https://doi.org/10.1186/s13068-015-0220-4"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.algal.2013.03.003", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1027492754"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1111/tpj.12682", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1028243195"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nm0898-882", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1029962141", 
              "https://doi.org/10.1038/nm0898-882"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1104/pp.113.214320", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1030516056"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1007/s10811-010-9608-5", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1033369912", 
              "https://doi.org/10.1007/s10811-010-9608-5"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1111/j.0022-3646.1989.00686.x", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1033559635"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/jxb/erv340", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1035542441"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1111/j.1757-1707.2010.01076.x", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1035725863"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/0960-0779(95)80025-c", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1037807675"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/0960-0779(95)80025-c", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1037807675"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1105/tpc.113.121418", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1038832084"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1002/(sici)1097-0290(19990620)63:6<705::aid-bit8>3.0.co;2-m", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1041156184"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1007/978-1-4615-8714-9_3", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1042981758", 
              "https://doi.org/10.1007/978-1-4615-8714-9_3"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1128/ec.00363-12", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1042989526"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1002/bit.22033", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1048369118"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1007/s00253-010-2753-6", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1048619457", 
              "https://doi.org/10.1007/s00253-010-2753-6"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nbt.1511", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1049469421", 
              "https://doi.org/10.1038/nbt.1511"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.3389/fmicb.2015.01042", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1051427714"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1128/ec.00203-09", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1052249688"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.biotechadv.2014.10.003", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1053166986"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.biotechadv.2012.04.007", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1053660932"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1021/ac401836j", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1055004613"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/pcp/pcv204", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1059972013"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1099/mic.0.000176", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1060394080"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1104/pp.106.2.503", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1060840492"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.18637/jss.v022.i04", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1068672326"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/ncomms14306", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1074207832", 
              "https://doi.org/10.1038/ncomms14306"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://app.dimensions.ai/details/publication/pub.1083027355", 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1111/mmi.13634", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1083398458"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.jprot.2017.03.010", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1084092013"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/s13068-017-0967-x", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1092751049", 
              "https://doi.org/10.1186/s13068-017-0967-x"
            ], 
            "type": "CreativeWork"
          }
        ], 
        "datePublished": "2019-12", 
        "datePublishedReg": "2019-12-01", 
        "description": "Background: Nannochloropsis oceanica belongs to a large group of photoautotrophic eukaryotic organisms that play important roles in fixation and cycling of atmospheric CO2. Its capability of storing solar energy and carbon dioxide in the form of triacylglycerol (TAG) of up to 60% of total weight under nitrogen deprivation stress sparked interest in its use for biofuel production. Phenotypes varying in lipid accumulation among an N. oceanica population can be disclosed by single-cell analysis/sorting using fluorescence-activated cell sorting (FACS); yet the phenomenon of single cell heterogeneity in an algae population remains to be fully understood at the molecular level. In this study, combination of FACS and proteomics was used for identification, quantification and differentiation of these heterogeneities on the molecular level.\nResults: For N. oceanica cultivated under nitrogen deplete (-N) and replete (+N) conditions, two groups differing in lipid content were distinguished. These differentiations could be recognized on the population as well as the single-cell levels; proteomics uncovered alterations in carbon fixation and flux, photosynthetic machinery, lipid storage and turnover in the populations. Although heterogeneity patterns have been affected by nitrogen supply and cultivation conditions of the N. oceanica populations, differentiation itself seems to be very robust against these factors: cultivation under +N, -N, in shaker bottles, and in a photo-bioreactor all split into two subpopulations. Intriguingly, population heterogeneity resumed after subpopulations were separately recultivated for a second round, refuting the possible development of genetic heterogeneity in the course of sorting and cultivation.\nConclusions: This work illustrates for the first time the feasibility of combining FACS and (prote)-omics for mechanistic understanding of phenotypic heterogeneity in lipid-producing microalgae. Such combinatorial method can facilitate molecular breeding and design of bioprocesses.", 
        "genre": "research_article", 
        "id": "sg:pub.10.1186/s13068-019-1361-7", 
        "inLanguage": [
          "en"
        ], 
        "isAccessibleForFree": true, 
        "isPartOf": [
          {
            "id": "sg:journal.1039046", 
            "issn": [
              "1754-6834"
            ], 
            "name": "Biotechnology for Biofuels", 
            "type": "Periodical"
          }, 
          {
            "issueNumber": "1", 
            "type": "PublicationIssue"
          }, 
          {
            "type": "PublicationVolume", 
            "volumeNumber": "12"
          }
        ], 
        "name": "Proteomic study uncovers molecular principles of single-cell-level phenotypic heterogeneity in lipid storage of Nannochloropsis oceanica", 
        "pagination": "21", 
        "productId": [
          {
            "name": "readcube_id", 
            "type": "PropertyValue", 
            "value": [
              "4074b2d16a57ffafd19288cd246db0190f82a1b9092d9a16dd22045c343e6527"
            ]
          }, 
          {
            "name": "pubmed_id", 
            "type": "PropertyValue", 
            "value": [
              "30740142"
            ]
          }, 
          {
            "name": "nlm_unique_id", 
            "type": "PropertyValue", 
            "value": [
              "101316935"
            ]
          }, 
          {
            "name": "doi", 
            "type": "PropertyValue", 
            "value": [
              "10.1186/s13068-019-1361-7"
            ]
          }, 
          {
            "name": "dimensions_id", 
            "type": "PropertyValue", 
            "value": [
              "pub.1111909569"
            ]
          }
        ], 
        "sameAs": [
          "https://doi.org/10.1186/s13068-019-1361-7", 
          "https://app.dimensions.ai/details/publication/pub.1111909569"
        ], 
        "sdDataset": "articles", 
        "sdDatePublished": "2019-04-11T09:04", 
        "sdLicense": "https://scigraph.springernature.com/explorer/license/", 
        "sdPublisher": {
          "name": "Springer Nature - SN SciGraph project", 
          "type": "Organization"
        }, 
        "sdSource": "s3://com-uberresearch-data-dimensions-target-20181106-alternative/cleanup/v134/2549eaecd7973599484d7c17b260dba0a4ecb94b/merge/v9/a6c9fde33151104705d4d7ff012ea9563521a3ce/jats-lookup/v90/0000000333_0000000333/records_41734_00000000.jsonl", 
        "type": "ScholarlyArticle", 
        "url": "https://link.springer.com/10.1186%2Fs13068-019-1361-7"
      }
    ]
     

    Download the RDF metadata as:  json-ld nt turtle xml License info

    HOW TO GET THIS DATA PROGRAMMATICALLY:

    JSON-LD is a popular format for linked data which is fully compatible with JSON.

    curl -H 'Accept: application/ld+json' 'https://scigraph.springernature.com/pub.10.1186/s13068-019-1361-7'

    N-Triples is a line-based linked data format ideal for batch operations.

    curl -H 'Accept: application/n-triples' 'https://scigraph.springernature.com/pub.10.1186/s13068-019-1361-7'

    Turtle is a human-readable linked data format.

    curl -H 'Accept: text/turtle' 'https://scigraph.springernature.com/pub.10.1186/s13068-019-1361-7'

    RDF/XML is a standard XML format for linked data.

    curl -H 'Accept: application/rdf+xml' 'https://scigraph.springernature.com/pub.10.1186/s13068-019-1361-7'


     

    This table displays all metadata directly associated to this object as RDF triples.

    263 TRIPLES      21 PREDICATES      77 URIs      21 LITERALS      9 BLANK NODES

    Subject Predicate Object
    1 sg:pub.10.1186/s13068-019-1361-7 schema:about anzsrc-for:06
    2 anzsrc-for:0601
    3 schema:author Nf8526428a93d47a2bc06cd628be6d6ff
    4 schema:citation sg:pub.10.1007/978-1-4615-8714-9_3
    5 sg:pub.10.1007/s00253-010-2753-6
    6 sg:pub.10.1007/s10811-010-9608-5
    7 sg:pub.10.1007/s10811-011-9768-y
    8 sg:pub.10.1038/nbt.1511
    9 sg:pub.10.1038/nchembio.436
    10 sg:pub.10.1038/ncomms14306
    11 sg:pub.10.1038/nm0898-882
    12 sg:pub.10.1038/nmicrobiol.2016.124
    13 sg:pub.10.1186/1754-6834-7-58
    14 sg:pub.10.1186/s13068-015-0220-4
    15 sg:pub.10.1186/s13068-017-0967-x
    16 https://app.dimensions.ai/details/publication/pub.1083027355
    17 https://doi.org/10.1002/(sici)1097-0290(19990620)63:6<705::aid-bit8>3.0.co;2-m
    18 https://doi.org/10.1002/bit.22033
    19 https://doi.org/10.1002/cyto.a.20683
    20 https://doi.org/10.1016/0960-0779(95)80025-c
    21 https://doi.org/10.1016/j.algal.2013.03.003
    22 https://doi.org/10.1016/j.biortech.2014.01.017
    23 https://doi.org/10.1016/j.biotechadv.2012.04.007
    24 https://doi.org/10.1016/j.biotechadv.2014.10.003
    25 https://doi.org/10.1016/j.jprot.2017.03.010
    26 https://doi.org/10.1016/j.mimet.2006.07.005
    27 https://doi.org/10.1016/j.ymben.2015.06.008
    28 https://doi.org/10.1021/ac401836j
    29 https://doi.org/10.1037/1082-989x.10.1.21
    30 https://doi.org/10.1073/pnas.1610758113
    31 https://doi.org/10.1074/mcp.m113.031591
    32 https://doi.org/10.1093/jxb/erv340
    33 https://doi.org/10.1093/nar/gkw880
    34 https://doi.org/10.1093/pcp/pcv204
    35 https://doi.org/10.1099/mic.0.000176
    36 https://doi.org/10.1104/pp.106.2.503
    37 https://doi.org/10.1104/pp.113.214320
    38 https://doi.org/10.1105/tpc.113.121418
    39 https://doi.org/10.1111/j.0022-3646.1989.00686.x
    40 https://doi.org/10.1111/j.1757-1707.2010.01076.x
    41 https://doi.org/10.1111/mmi.13634
    42 https://doi.org/10.1111/nph.13728
    43 https://doi.org/10.1111/nph.13843
    44 https://doi.org/10.1111/tpj.12682
    45 https://doi.org/10.1128/ec.00203-09
    46 https://doi.org/10.1128/ec.00363-12
    47 https://doi.org/10.1128/jb.00310-08
    48 https://doi.org/10.1371/journal.pone.0085731
    49 https://doi.org/10.1371/journal.pone.0160711
    50 https://doi.org/10.18637/jss.v022.i04
    51 https://doi.org/10.3389/fmicb.2015.01042
    52 schema:datePublished 2019-12
    53 schema:datePublishedReg 2019-12-01
    54 schema:description Background: Nannochloropsis oceanica belongs to a large group of photoautotrophic eukaryotic organisms that play important roles in fixation and cycling of atmospheric CO2. Its capability of storing solar energy and carbon dioxide in the form of triacylglycerol (TAG) of up to 60% of total weight under nitrogen deprivation stress sparked interest in its use for biofuel production. Phenotypes varying in lipid accumulation among an N. oceanica population can be disclosed by single-cell analysis/sorting using fluorescence-activated cell sorting (FACS); yet the phenomenon of single cell heterogeneity in an algae population remains to be fully understood at the molecular level. In this study, combination of FACS and proteomics was used for identification, quantification and differentiation of these heterogeneities on the molecular level. Results: For N. oceanica cultivated under nitrogen deplete (-N) and replete (+N) conditions, two groups differing in lipid content were distinguished. These differentiations could be recognized on the population as well as the single-cell levels; proteomics uncovered alterations in carbon fixation and flux, photosynthetic machinery, lipid storage and turnover in the populations. Although heterogeneity patterns have been affected by nitrogen supply and cultivation conditions of the N. oceanica populations, differentiation itself seems to be very robust against these factors: cultivation under +N, -N, in shaker bottles, and in a photo-bioreactor all split into two subpopulations. Intriguingly, population heterogeneity resumed after subpopulations were separately recultivated for a second round, refuting the possible development of genetic heterogeneity in the course of sorting and cultivation. Conclusions: This work illustrates for the first time the feasibility of combining FACS and (prote)-omics for mechanistic understanding of phenotypic heterogeneity in lipid-producing microalgae. Such combinatorial method can facilitate molecular breeding and design of bioprocesses.
    55 schema:genre research_article
    56 schema:inLanguage en
    57 schema:isAccessibleForFree true
    58 schema:isPartOf N2ba5053e1153472580b1a8ef1443e4fa
    59 Ndbc4c2c768604f7bbd053108f154352c
    60 sg:journal.1039046
    61 schema:name Proteomic study uncovers molecular principles of single-cell-level phenotypic heterogeneity in lipid storage of Nannochloropsis oceanica
    62 schema:pagination 21
    63 schema:productId N23288fd10abe461380fbed46f86e0727
    64 N52152d09dc814dbbbe3fe7117b391ddc
    65 N7da925b2994240ffb9aea0ed265e38d4
    66 N8667b02bb2c4480b94d691ba593b13c1
    67 Nbcfdfc372b6d425b90954b58b5b0ec2f
    68 schema:sameAs https://app.dimensions.ai/details/publication/pub.1111909569
    69 https://doi.org/10.1186/s13068-019-1361-7
    70 schema:sdDatePublished 2019-04-11T09:04
    71 schema:sdLicense https://scigraph.springernature.com/explorer/license/
    72 schema:sdPublisher N1638fdcf00cc409d9dc5498c24dbadce
    73 schema:url https://link.springer.com/10.1186%2Fs13068-019-1361-7
    74 sgo:license sg:explorer/license/
    75 sgo:sdDataset articles
    76 rdf:type schema:ScholarlyArticle
    77 N16163e97ede94df4a59ca6c45aa15ac6 rdf:first N194d39cc2e914aa4a712da40051ff07c
    78 rdf:rest N49b5421f31bf429ea04c85ae9a9a3245
    79 N1638fdcf00cc409d9dc5498c24dbadce schema:name Springer Nature - SN SciGraph project
    80 rdf:type schema:Organization
    81 N194d39cc2e914aa4a712da40051ff07c schema:affiliation https://www.grid.ac/institutes/grid.458500.c
    82 schema:familyName You
    83 schema:givenName Wuxin
    84 rdf:type schema:Person
    85 N23288fd10abe461380fbed46f86e0727 schema:name pubmed_id
    86 schema:value 30740142
    87 rdf:type schema:PropertyValue
    88 N2ba5053e1153472580b1a8ef1443e4fa schema:volumeNumber 12
    89 rdf:type schema:PublicationVolume
    90 N392bccd6c4c8416c9bcf66323373a4ac schema:affiliation https://www.grid.ac/institutes/grid.458500.c
    91 schema:familyName Xu
    92 schema:givenName Jian
    93 rdf:type schema:Person
    94 N49b5421f31bf429ea04c85ae9a9a3245 rdf:first N392bccd6c4c8416c9bcf66323373a4ac
    95 rdf:rest Nc195a1ccee754fdb87880b31a13c2b45
    96 N52152d09dc814dbbbe3fe7117b391ddc schema:name readcube_id
    97 schema:value 4074b2d16a57ffafd19288cd246db0190f82a1b9092d9a16dd22045c343e6527
    98 rdf:type schema:PropertyValue
    99 N718492b3d36a48bb926f1b38c6218639 rdf:first N83ba6366dbd74b0ebe1a20715a9718db
    100 rdf:rest rdf:nil
    101 N7da925b2994240ffb9aea0ed265e38d4 schema:name nlm_unique_id
    102 schema:value 101316935
    103 rdf:type schema:PropertyValue
    104 N83ba6366dbd74b0ebe1a20715a9718db schema:affiliation https://www.grid.ac/institutes/grid.11201.33
    105 schema:familyName Poetsch
    106 schema:givenName Ansgar
    107 rdf:type schema:Person
    108 N8667b02bb2c4480b94d691ba593b13c1 schema:name dimensions_id
    109 schema:value pub.1111909569
    110 rdf:type schema:PropertyValue
    111 N8de9b1dc135947e3a355a5f971b20d2a schema:affiliation https://www.grid.ac/institutes/grid.33199.31
    112 schema:familyName Ning
    113 schema:givenName Kang
    114 rdf:type schema:Person
    115 N94fd5148b6734a7eab8636dd0d3d79dd schema:affiliation https://www.grid.ac/institutes/grid.5570.7
    116 schema:familyName Harst
    117 schema:givenName Andreas
    118 rdf:type schema:Person
    119 N95ef4eb226e44cb289ef302d3592f040 rdf:first N94fd5148b6734a7eab8636dd0d3d79dd
    120 rdf:rest N16163e97ede94df4a59ca6c45aa15ac6
    121 Nbcfdfc372b6d425b90954b58b5b0ec2f schema:name doi
    122 schema:value 10.1186/s13068-019-1361-7
    123 rdf:type schema:PropertyValue
    124 Nc195a1ccee754fdb87880b31a13c2b45 rdf:first N8de9b1dc135947e3a355a5f971b20d2a
    125 rdf:rest N718492b3d36a48bb926f1b38c6218639
    126 Ndbc4c2c768604f7bbd053108f154352c schema:issueNumber 1
    127 rdf:type schema:PublicationIssue
    128 Nf1da0ebb34b84e2cb2f85e539e07abb8 schema:affiliation https://www.grid.ac/institutes/grid.33199.31
    129 schema:familyName Chen
    130 schema:givenName Chaoyun
    131 rdf:type schema:Person
    132 Nf8526428a93d47a2bc06cd628be6d6ff rdf:first Nf1da0ebb34b84e2cb2f85e539e07abb8
    133 rdf:rest N95ef4eb226e44cb289ef302d3592f040
    134 anzsrc-for:06 schema:inDefinedTermSet anzsrc-for:
    135 schema:name Biological Sciences
    136 rdf:type schema:DefinedTerm
    137 anzsrc-for:0601 schema:inDefinedTermSet anzsrc-for:
    138 schema:name Biochemistry and Cell Biology
    139 rdf:type schema:DefinedTerm
    140 sg:journal.1039046 schema:issn 1754-6834
    141 schema:name Biotechnology for Biofuels
    142 rdf:type schema:Periodical
    143 sg:pub.10.1007/978-1-4615-8714-9_3 schema:sameAs https://app.dimensions.ai/details/publication/pub.1042981758
    144 https://doi.org/10.1007/978-1-4615-8714-9_3
    145 rdf:type schema:CreativeWork
    146 sg:pub.10.1007/s00253-010-2753-6 schema:sameAs https://app.dimensions.ai/details/publication/pub.1048619457
    147 https://doi.org/10.1007/s00253-010-2753-6
    148 rdf:type schema:CreativeWork
    149 sg:pub.10.1007/s10811-010-9608-5 schema:sameAs https://app.dimensions.ai/details/publication/pub.1033369912
    150 https://doi.org/10.1007/s10811-010-9608-5
    151 rdf:type schema:CreativeWork
    152 sg:pub.10.1007/s10811-011-9768-y schema:sameAs https://app.dimensions.ai/details/publication/pub.1023799797
    153 https://doi.org/10.1007/s10811-011-9768-y
    154 rdf:type schema:CreativeWork
    155 sg:pub.10.1038/nbt.1511 schema:sameAs https://app.dimensions.ai/details/publication/pub.1049469421
    156 https://doi.org/10.1038/nbt.1511
    157 rdf:type schema:CreativeWork
    158 sg:pub.10.1038/nchembio.436 schema:sameAs https://app.dimensions.ai/details/publication/pub.1003940702
    159 https://doi.org/10.1038/nchembio.436
    160 rdf:type schema:CreativeWork
    161 sg:pub.10.1038/ncomms14306 schema:sameAs https://app.dimensions.ai/details/publication/pub.1074207832
    162 https://doi.org/10.1038/ncomms14306
    163 rdf:type schema:CreativeWork
    164 sg:pub.10.1038/nm0898-882 schema:sameAs https://app.dimensions.ai/details/publication/pub.1029962141
    165 https://doi.org/10.1038/nm0898-882
    166 rdf:type schema:CreativeWork
    167 sg:pub.10.1038/nmicrobiol.2016.124 schema:sameAs https://app.dimensions.ai/details/publication/pub.1011179589
    168 https://doi.org/10.1038/nmicrobiol.2016.124
    169 rdf:type schema:CreativeWork
    170 sg:pub.10.1186/1754-6834-7-58 schema:sameAs https://app.dimensions.ai/details/publication/pub.1010497314
    171 https://doi.org/10.1186/1754-6834-7-58
    172 rdf:type schema:CreativeWork
    173 sg:pub.10.1186/s13068-015-0220-4 schema:sameAs https://app.dimensions.ai/details/publication/pub.1025480930
    174 https://doi.org/10.1186/s13068-015-0220-4
    175 rdf:type schema:CreativeWork
    176 sg:pub.10.1186/s13068-017-0967-x schema:sameAs https://app.dimensions.ai/details/publication/pub.1092751049
    177 https://doi.org/10.1186/s13068-017-0967-x
    178 rdf:type schema:CreativeWork
    179 https://app.dimensions.ai/details/publication/pub.1083027355 schema:CreativeWork
    180 https://doi.org/10.1002/(sici)1097-0290(19990620)63:6<705::aid-bit8>3.0.co;2-m schema:sameAs https://app.dimensions.ai/details/publication/pub.1041156184
    181 rdf:type schema:CreativeWork
    182 https://doi.org/10.1002/bit.22033 schema:sameAs https://app.dimensions.ai/details/publication/pub.1048369118
    183 rdf:type schema:CreativeWork
    184 https://doi.org/10.1002/cyto.a.20683 schema:sameAs https://app.dimensions.ai/details/publication/pub.1020721335
    185 rdf:type schema:CreativeWork
    186 https://doi.org/10.1016/0960-0779(95)80025-c schema:sameAs https://app.dimensions.ai/details/publication/pub.1037807675
    187 rdf:type schema:CreativeWork
    188 https://doi.org/10.1016/j.algal.2013.03.003 schema:sameAs https://app.dimensions.ai/details/publication/pub.1027492754
    189 rdf:type schema:CreativeWork
    190 https://doi.org/10.1016/j.biortech.2014.01.017 schema:sameAs https://app.dimensions.ai/details/publication/pub.1007821347
    191 rdf:type schema:CreativeWork
    192 https://doi.org/10.1016/j.biotechadv.2012.04.007 schema:sameAs https://app.dimensions.ai/details/publication/pub.1053660932
    193 rdf:type schema:CreativeWork
    194 https://doi.org/10.1016/j.biotechadv.2014.10.003 schema:sameAs https://app.dimensions.ai/details/publication/pub.1053166986
    195 rdf:type schema:CreativeWork
    196 https://doi.org/10.1016/j.jprot.2017.03.010 schema:sameAs https://app.dimensions.ai/details/publication/pub.1084092013
    197 rdf:type schema:CreativeWork
    198 https://doi.org/10.1016/j.mimet.2006.07.005 schema:sameAs https://app.dimensions.ai/details/publication/pub.1001020024
    199 rdf:type schema:CreativeWork
    200 https://doi.org/10.1016/j.ymben.2015.06.008 schema:sameAs https://app.dimensions.ai/details/publication/pub.1006710224
    201 rdf:type schema:CreativeWork
    202 https://doi.org/10.1021/ac401836j schema:sameAs https://app.dimensions.ai/details/publication/pub.1055004613
    203 rdf:type schema:CreativeWork
    204 https://doi.org/10.1037/1082-989x.10.1.21 schema:sameAs https://app.dimensions.ai/details/publication/pub.1015425693
    205 rdf:type schema:CreativeWork
    206 https://doi.org/10.1073/pnas.1610758113 schema:sameAs https://app.dimensions.ai/details/publication/pub.1017987367
    207 rdf:type schema:CreativeWork
    208 https://doi.org/10.1074/mcp.m113.031591 schema:sameAs https://app.dimensions.ai/details/publication/pub.1019972763
    209 rdf:type schema:CreativeWork
    210 https://doi.org/10.1093/jxb/erv340 schema:sameAs https://app.dimensions.ai/details/publication/pub.1035542441
    211 rdf:type schema:CreativeWork
    212 https://doi.org/10.1093/nar/gkw880 schema:sameAs https://app.dimensions.ai/details/publication/pub.1022739704
    213 rdf:type schema:CreativeWork
    214 https://doi.org/10.1093/pcp/pcv204 schema:sameAs https://app.dimensions.ai/details/publication/pub.1059972013
    215 rdf:type schema:CreativeWork
    216 https://doi.org/10.1099/mic.0.000176 schema:sameAs https://app.dimensions.ai/details/publication/pub.1060394080
    217 rdf:type schema:CreativeWork
    218 https://doi.org/10.1104/pp.106.2.503 schema:sameAs https://app.dimensions.ai/details/publication/pub.1060840492
    219 rdf:type schema:CreativeWork
    220 https://doi.org/10.1104/pp.113.214320 schema:sameAs https://app.dimensions.ai/details/publication/pub.1030516056
    221 rdf:type schema:CreativeWork
    222 https://doi.org/10.1105/tpc.113.121418 schema:sameAs https://app.dimensions.ai/details/publication/pub.1038832084
    223 rdf:type schema:CreativeWork
    224 https://doi.org/10.1111/j.0022-3646.1989.00686.x schema:sameAs https://app.dimensions.ai/details/publication/pub.1033559635
    225 rdf:type schema:CreativeWork
    226 https://doi.org/10.1111/j.1757-1707.2010.01076.x schema:sameAs https://app.dimensions.ai/details/publication/pub.1035725863
    227 rdf:type schema:CreativeWork
    228 https://doi.org/10.1111/mmi.13634 schema:sameAs https://app.dimensions.ai/details/publication/pub.1083398458
    229 rdf:type schema:CreativeWork
    230 https://doi.org/10.1111/nph.13728 schema:sameAs https://app.dimensions.ai/details/publication/pub.1010046819
    231 rdf:type schema:CreativeWork
    232 https://doi.org/10.1111/nph.13843 schema:sameAs https://app.dimensions.ai/details/publication/pub.1017663686
    233 rdf:type schema:CreativeWork
    234 https://doi.org/10.1111/tpj.12682 schema:sameAs https://app.dimensions.ai/details/publication/pub.1028243195
    235 rdf:type schema:CreativeWork
    236 https://doi.org/10.1128/ec.00203-09 schema:sameAs https://app.dimensions.ai/details/publication/pub.1052249688
    237 rdf:type schema:CreativeWork
    238 https://doi.org/10.1128/ec.00363-12 schema:sameAs https://app.dimensions.ai/details/publication/pub.1042989526
    239 rdf:type schema:CreativeWork
    240 https://doi.org/10.1128/jb.00310-08 schema:sameAs https://app.dimensions.ai/details/publication/pub.1016525614
    241 rdf:type schema:CreativeWork
    242 https://doi.org/10.1371/journal.pone.0085731 schema:sameAs https://app.dimensions.ai/details/publication/pub.1000154881
    243 rdf:type schema:CreativeWork
    244 https://doi.org/10.1371/journal.pone.0160711 schema:sameAs https://app.dimensions.ai/details/publication/pub.1006327278
    245 rdf:type schema:CreativeWork
    246 https://doi.org/10.18637/jss.v022.i04 schema:sameAs https://app.dimensions.ai/details/publication/pub.1068672326
    247 rdf:type schema:CreativeWork
    248 https://doi.org/10.3389/fmicb.2015.01042 schema:sameAs https://app.dimensions.ai/details/publication/pub.1051427714
    249 rdf:type schema:CreativeWork
    250 https://www.grid.ac/institutes/grid.11201.33 schema:alternateName Plymouth University
    251 schema:name Plant Biochemistry, Ruhr University Bochum, 44801, Bochum, Germany
    252 School of Biomedical and Healthcare Sciences, Plymouth University, PL4 8AA, Plymouth, UK
    253 rdf:type schema:Organization
    254 https://www.grid.ac/institutes/grid.33199.31 schema:alternateName Huazhong University of Science and Technology
    255 schema:name Key Laboratory of Molecular Biophysics of the Ministry of Education, Hubei Key Laboratory of Bioinformatics and Molecular-imaging, Department of Bioinformatics and Systems Biology, College of Life Science and Technology, Huazhong University of Science and Technology, 430074, Wuhan, Hubei, China
    256 rdf:type schema:Organization
    257 https://www.grid.ac/institutes/grid.458500.c schema:alternateName Qingdao Institute of Bioenergy and Bioprocess Technology
    258 schema:name Plant Biochemistry, Ruhr University Bochum, 44801, Bochum, Germany
    259 Single-Cell Center, CAS Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, 266101, Qingdao, Shandong, China
    260 rdf:type schema:Organization
    261 https://www.grid.ac/institutes/grid.5570.7 schema:alternateName Ruhr University Bochum
    262 schema:name Plant Biochemistry, Ruhr University Bochum, 44801, Bochum, Germany
    263 rdf:type schema:Organization
     




    Preview window. Press ESC to close (or click here)


    ...