Gene expression during bacterivorous growth of a widespread marine heterotrophic flagellate

  • 1.

    Sherr BF, Sherr EB, Caron D, Vaulot D, Worden A. Oceanic protists. Oceanography. 2007;20:130–34.


    Google Scholar
     

  • 2.

    Worden AZ, Follows MJ, Giovannoni SJ, Wilken S, Zimmerman AE, Keeling PJ. Rethinking the marine carbon cycle: factoring in the multifarious lifestyles of microbes. Science. 2015;347:1257594.

    PubMed 

    Google Scholar
     

  • 3.

    Jürgens K, Massana R. Protistan Grazing on Marine Bacterioplankton. In: D.L. Kirchman [ed.], Microbial ecology of the oceans. John Wiley & Sons, Inc; Hoboken, New Jersey, 2008. p. 383–441.

  • 4.

    Pernthaler J. Predation on prokaryotes in the water column and its ecological implications. Nat Rev Microbiol. 2005;3:537–46.

    CAS 
    PubMed 

    Google Scholar
     

  • 5.

    Boenigk J, Arndt H. Bacterivory by heterotrophic flagellates: community structure and feeding strategies. Ant van Leeuw. 2002;81:465–80.


    Google Scholar
     

  • 6.

    Vørs N, Buck KR, Chavez FP, Eikrem W, Hansen LE, Østergaard JB, et al. Nanoplankton of the equatorial Pacific with emphasis on the heterotrophic protists. Deep-Sea Res II. 1995;42:585–602.


    Google Scholar
     

  • 7.

    Massana R, Guillou L, Díez B, Pedrós-Alió C. Unveiling the organisms behind novel eukaryotic ribosomal DNA sequences from the ocean. Appl Environ Microbiol. 2002;68:4554–58.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 8.

    Rodríguez-Martínez R, Rocap G, Logares R, Romac S, Massana R. Low evolutionary diversification in a widespread and abundant uncultured protist (MAST-4). Mol Biol Evol. 2012;29:1393–406.

    PubMed 

    Google Scholar
     

  • 9.

    del Campo J, Balagué V, Forn I, Lekunberri I, Massana R. Culturing bias in marine heterotrophic flagellates analyzed through seawater enrichment incubations. Micro Ecol. 2013;66:489–99.

    CAS 

    Google Scholar
     

  • 10.

    Caron DA, Alexander H, Allen AE, Archibald JM, Armbrust EV, Bachy C, et al. Probing the evolution, ecology and physiology of marine protists using transcriptomics. Nat Rev Micro. 2017;15:6–20.

    CAS 

    Google Scholar
     

  • 11.

    Yutin N, Wolf MY, Wolf YI, Koonin EV. The origins of phagocytosis and eukaryogenesis. Biol Direct. 2009;4:9.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 12.

    Keeling PJ. The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Annu Rev Plant Biol. 2013;64:583–607.

    CAS 

    Google Scholar
     

  • 13.

    Martin WF, Tielens AGM, Mentel M, Garg SG, Gould SB. The physiology of phagocytosis in the context of mitochondrial origin. Micro Mol Biol Rev. 2017;81:e00008–17.

    CAS 

    Google Scholar
     

  • 14.

    Rosales C, Uribe-Querol E. Phagocytosis: a fundamental process in immunity. BioMed Res Int. 2017;2017:9042851.

  • 15.

    Gotthardt D, Warnatz HJ, Henschel O, Brückert F, Schleicher M, Soldati T. (2002). High-resolution dissection of phagosome maturation reveals distinct membrane trafficking phases. Mol Biol Cell. 2002;13:3508–20.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 16.

    Niedergang F, Grinstein S. How to build a phagosome: new concepts for an old process. Curr Opin Cell Biol. 2018;50:57–63.

    CAS 
    PubMed 

    Google Scholar
     

  • 17.

    Kanehisa M, Sato Y, Furumichi M, Morishima K, Tanabe M. New approach for understanding genome variations in KEGG. Nucleic Acids Res. 2019;47:D590–5.

    CAS 
    PubMed 

    Google Scholar
     

  • 18.

    Bozzaro S, Bucci C, Steinert M. Phagocytosis and host-pathogen interactions in Dictyostelium with a look at macrophages. Int Rev Cell Mol Biol. 2008;271:253–300.

    CAS 
    PubMed 

    Google Scholar
     

  • 19.

    Jacobs ME, DeSouza LV, Samaranayake H, Pearlman RE, Siu KWM, Klobutcher LA. The Tetrahymena thermophila phagosome proteome. Eukaryot Cell. 2006;5:1990–2000.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 20.

    Boulais J, Trost M, Landry CR, Dieckmann R, Levy ED, Soldati T, et al. Molecular characterization of the evolution of phagosomes. Mol Syst Biol. 2010;6:423.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 21.

    Lie AAY, Liu Z, Terrado R, Tatters AO, Heidelberg KB, Caron DA. Effect of light and prey availability on gene expression of the mixotrophic chrysophyte Ochromonas sp. BMC Genomics. 2017;18:163.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 22.

    Rubin ET, Cheng S, Montalbano AL, Menden-Deuen S, Rynearson TA. Transcriptomic response to feeding and starvation in a herbivorous dinoflagellate. Front Mar Sci. 2019;6:246.


    Google Scholar
     

  • 23.

    Fenchel T, Patterson DJ. Cafeteria roenbergensis nov. gen., nov. sp., a heterotrophic microflagellate from marine plankton. Mar Micro Food Webs. 1988;3:9–19.


    Google Scholar
     

  • 24.

    Schoenle A, Hohlfeld M, Rosse M, Filz P, Wylezich C, Nitsche F, et al. Global comparison of bicosoecid Cafeteria-like flagellates from the deep ocean and surface waters, with reorganization of the family Cafeteriaceae. Eur J Protistol. 2020;73:125665.

    PubMed 

    Google Scholar
     

  • 25.

    Keeling PJ, Burki F, Wilcox HM, Allam B, Allen EE, Amaral- Zettler LA, et al. The marine microbial eukaryote transcriptome Sequencing Project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biol. 2014;12:e1001889.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 26.

    Hackl T, Martin R, Barenhoff K, Duponchel S, Heider D, Fischer MG. Four high-quality draft genome assemblies of the marine heterotrophic nanoflagellate Cafeteria roenbergensis. Sci Data. 2020;7:29.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 27.

    Anderson R, Kjelleberg S, Mcdougald D, Jürgens K. Species-specific patterns in the vulnerability of carbon-starved bacteria to protist grazing. Aquat Micro Ecol. 2011;64:105–16.


    Google Scholar
     

  • 28.

    de Corte D, Paredes G, Yokokawa T, Sintes E, Herndl GJ. Differential response of Cafeteria roenbergensis to different bacterial and archaeal characteristics. Micro Ecol. 2019;78:1–5.


    Google Scholar
     

  • 29.

    Massana R, del Campo J, Dinter C, Sommaruga R. Crash of a population of the marine heterotrophic flagellate Cafeteria roenbergensis by viral infection. Environ Microbiol. 2007;9:2660–69.

    CAS 
    PubMed 

    Google Scholar
     

  • 30.

    Logares R, Deutschmann IM, Junger PC, Giner CR, Krabberød AK, Schmidt TSB, et al. Disentangling the mechanisms shaping the surface ocean microbiota. Microbiome 2020;8:55.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 31.

    Giner CR, Pernice MC, Balagué V, Duarte CM, Gasol JM, Logares R, et al. Marked changes in diversity and relative activity of picoeukaryotes with depth in the world ocean. ISME J. 2020;14:437–49.

    PubMed 

    Google Scholar
     

  • 32.

    Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Meth. 2016;13:581–83.

    CAS 

    Google Scholar
     

  • 33.

    Obiol A, Giner CR, Sánchez P, Duarte CM, Acinas SG, Massana R. A metagenomic assessment of microbial eukaryotic diversity in the global ocean. Mol Ecol Res. 2020;20:718–31.

    CAS 

    Google Scholar
     

  • 34.

    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–10.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 35.

    Mangot J-F, Forn I, Obiol A, Massana R. Constant abundances of ubiquitous uncultured protists in the open sea assessed by automated microscopy. Environ Microbiol. 2018;20:3876–89.

    CAS 
    PubMed 

    Google Scholar
     

  • 36.

    Lekunberri I, Gasol JM, Acinas SG, Gómez-Consarnau L, Crespo BG, Casamayor EO, et al. The phylogenetic and ecological context of cultured and whole genome-sequenced planktonic bacteria from the coastal NW Mediterranean Sea. Syst Appl Microbiol. 2014;37:216–28.

    PubMed 

    Google Scholar
     

  • 37.

    Porter KG, Feig YS. The use of DAPI for identifying aquatic microfloral. Limnol Oceanogr. 1980;25:943–48.


    Google Scholar
     

  • 38.

    González JM, Suttle CA. Grazing by marine nanoflagellates on viruses and virus-sized particles: ingestion and digestion. Mar Ecol Prog Ser. 1993;94:1–10.


    Google Scholar
     

  • 39.

    Frost BW. Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnol Oceanogr. 1972;17:805–15.


    Google Scholar
     

  • 40.

    Heinbokel JF. Studies on the functional role of tintinnids in the Southern California Bight. I. Grazing and growth rates in laboratory cultures. Mar Biol. 1978;47:177–89.


    Google Scholar
     

  • 41.

    Menden-Deuer S, Lessard EJ. 2000. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol Oceanogr. 2000;45:569–79.

    CAS 

    Google Scholar
     

  • 42.

    Picelli S, Faridani OR, Björklund Å, Winberg G, Sagasser S, Sandberg R. Full-length RNA-seq from single cells using Smart-seq2. Nat Protoc. 2014;9:171–81.

    CAS 
    PubMed 

    Google Scholar
     

  • 43.

    Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014;30:2114–20.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 44.

    Langmead B, Salzberg S. Fast gapped-read alignment with Bowtie 2. Nat Meth. 2012;9:357–59.

    CAS 

    Google Scholar
     

  • 45.

    Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 2013;8:1494–512.

    CAS 
    PubMed 

    Google Scholar
     

  • 46.

    The UniProt Consortium. UniProt: a worldwide hub of protein knowledge. Nucleic Acids Res. 2019;47:D506–15.


    Google Scholar
     

  • 47.

    Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, et al. The Pfam protein families database. Nucleic Acids Res. 2012;40:D290–301.

    CAS 
    PubMed 

    Google Scholar
     

  • 48.

    Powell S, Szklarczyk D, Trachana K, Roth A, Kuhn M, Muller J, et al. eggNOG v3.0: orthologous groups covering 1133 organisms at 41 different taxonomic ranges. Nucleic Acids Res. 2012;40:D284–9.

    CAS 
    PubMed 

    Google Scholar
     

  • 49.

    Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinforma. 2011;12:323.

    CAS 

    Google Scholar
     

  • 50.

    Waterhouse RM, Seppey M, Simão FA, Manni M, Ioannidis P, Klioutchnikov G, et al. BUSCO applications from quality assessments to gene prediction and phylogenomics. Mol Biol Evol. 2018;35:543–48.

    CAS 
    PubMed 

    Google Scholar
     

  • 51.

    van Bel M, Proost S, van Neste C, Deforce D, van de Peer Y, Vandepoele K. TRAPID, an efficient online tool for the functional and comparative analysis of de novo RNA-Seq transcriptomes. Genome Biol. 2013;14:R134.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 52.

    Finn RD, Attwood TK, Babbitt PC, Bateman A, Bork P, Bridge AJ, et al. InterPro in 2017-beyond protein family and domain annotations. Nucleic Acids Res. 2017;45:D190–9.

    CAS 
    PubMed 

    Google Scholar
     

  • 53.

    Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Meth. 2015;12:59–60.

    CAS 

    Google Scholar
     

  • 54.

    Van Bel M, Diels T, Vancaester E, Kreft L, Botzki A, Van de Peer Y, et al. PLAZA 4.0: an integrative resource for functional, evolutionary and comparative plant genomics. Nucleic Acids Res. 2018;46:D1190–6.

    PubMed 

    Google Scholar
     

  • 55.

    McCarthy DJ, Chen Y, Smyth GK. Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res. 2012;40:4288–97.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 56.

    Zinger L, Gobet A, Pommier T. Two decades of describing the unseen majority of aquatic microbial diversity. Mol Ecol. 2012;21:1878–96.

    PubMed 

    Google Scholar
     

  • 57.

    Pernice MC, Forn I, Gomes A, Lara E, Alonso-Sáez L, Arrieta JM, et al. Global abundance of planktonic heterotrophic protists in the deep ocean. ISME J. 2015;9:782–92.

    CAS 
    PubMed 

    Google Scholar
     

  • 58.

    Eccleston-Parry JD, Leadbeater BSC. A comparison of the growth-kinetics of 6 marine heterotrophic nanoflagellates fed with one bacterial species. Mar Ecol Prog Ser. 1994;105:167–77.


    Google Scholar
     

  • 59.

    Arndt H, Hausmann K, Wolf M. Deep-sea heterotrophic nanoflagellates of the Eastern Mediterranean Sea: qualitative and quantitative aspects of their pelagic and benthic occurrence. Mar Ecol Prog Ser. 2003;256:45–56.


    Google Scholar
     

  • 60.

    Azam F, Long RA. Sea snow microcosms. Nature 2001;414:495–98.

    CAS 
    PubMed 

    Google Scholar
     

  • 61.

    Fenchel T. Ecology of protozoa: The biology of free-living phagotrophic protists. Science Tech Publishers, Madison and Springer-Verlag; Madison, Wisconsin, 1987.

  • 62.

    Mestre M, Ruiz-González C, Logares R, Duarte CM, Gasol JM, Sala MM. Sinking particles promote vertical connectivity in the ocean microbiome. Proc Natl Acad Sci USA. 2018;115:E6799–807.

    CAS 
    PubMed 

    Google Scholar
     

  • 63.

    Beisser D, Graupner N, Bock C, Wodniok S, Grosmann L, Vos M, et al. Comprehensive transcriptome analysis provides new insights into nutritional strategies and phylogenetic relationships of chrysophytes. PeerJ. 2017;5:e2832.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 64.

    Liu Z, Campbell V, Heidelberg KB, Caron DA. Gene expression characterizes different nutritional strategies among three mixotrophic protists. FEMS Micro Ecol. 2016;92:fiw106.


    Google Scholar
     

  • 65.

    Garba L, Ali MSM, Oslan SN, RNZRB AbdulRahman. Review on fatty acid desaturases and their roles in temperature acclimatisation. J Appl Sci. 2017;17:282–95.

    CAS 

    Google Scholar
     

  • 66.

    Cheng W, Lin M, Qiu M, Kong L, Xu Y, Li Y, et al. Chitin synthase is involved in vegetative growth, asexual reproduction and pathogenesis of Phytophthora capsici and Phytophthora. Environ Microbiol. 2019;21:4537–47.

    CAS 
    PubMed 

    Google Scholar
     

  • 67.

    Rawlings ND, Barrett AJ. Families of cysteine peptidases. Methods Enzymol. 1994;244:461–86.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 68.

    Rawlings ND, Barrett AJ, Finn R. Twenty years of the MEROPS database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res. 2015;44:D343–50.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 69.

    Baltscheffsky M, Schultz A, Baltscheffsky H. H+-proton-pumping inorganic pyrophosphatase: a tightly membrane-bound family. FEBS Lett. 1999;457:527–33.

    CAS 
    PubMed 

    Google Scholar
     

  • 70.

    Labarre A, Obiol A, Wilken S, Forn I, Massana R. Expression of genes involved in phagocytosis in uncultured heterotrophic flagellates. Limnol Oceanogr. 2020;65:S149–60.

    CAS 

    Google Scholar
     

  • 71.

    Minakami R, Sumimotoa H. Phagocytosis-coupled activation of the superoxide-producing phagocyte oxidase, a member of the NADPH oxidase (nox) family. Int J Hematol. 2006;84:193–98.

    CAS 
    PubMed 

    Google Scholar
     

  • Source Article