Diatoms are an ecologically fundamental and highly diverse group of algae, dominating marine primary production in both open-water and coastal communities. The diatoms include both centric species, which may have radial or polar symmetry, and the pennates, which include raphid and araphid species and arose within the centric lineage. Here, we use combined microscopic and molecular information to reclassify a diatom strain CCMP470, previously annotated as a radial centric species related to Leptocylindrus danicus, as an araphid pennate species in the staurosiroid lineage, within the genus Plagiostriata. CCMP470 shares key ultrastructural features with Plagiostriata taxa, such as the presence of a sternum with parallel striae, and the presence of a highly reduced labiate process on its valve; and this evolutionary position is robustly supported by multigene phylogenetic analysis. We additionally present a draft genome of CCMP470, which is the first genome available for a staurosiroid lineage. 270 Pfams (19%) found in the CCMP470 genome are not known in other diatom genomes, which otherwise does not hold big novelties compared to genomes of non-staurosiroid diatoms. Notably, our DNA library contains the genome of a bacterium within the Rhodobacterales, an alpha-proteobacterial lineage known frequently to associate with algae. We demonstrate the presence of commensal alpha-proteobacterial sequences in other published algal genome and transcriptome datasets, which may indicate widespread and persistent co-occurrence.

Biology Centre CAS Institute of Parasitology Ceske Budejovice Czech Republic

Centre for Comparative Genomics and Evolutionary Bioinformatics Department of Biochemistry and Molecular Biology Dalhousie University Halifax Canada

Charles University Faculty of Science BIOCEV Prague Czech Republic

Fukui Prefectural University Fukui 917 0003 Japan

Génomique Métabolique Genoscope Institut Francois Jacob CEA CNRS Univ Evry Université Paris Saclay 91057 Evry France

Institut de Biologie de l'ENS Département de biologie École normale supérieure CNRS INSERM Université PSL 75005 Paris France

Institute for Food and Agricultural Research and Technology E 43540 Sant Carles de la Ràpita Catalunya Spain

Royal Botanic Garden Edinburgh EH3 5LR Scotland UK

Stazione Zoologica Anton Dohrn Villa Comunale 80121 Napoli Italy

Stony Brook University School of Marine and Atmospheric Sciences Southampton New York USA

Université de Nantes CNRS UFIP UMR 6286 F 44000 Nantes France

University of South Bohemia Faculty of Science Ceske Budejovice Czech Republic

See more in PubMed

Falkowski PG, Barber RT, Smetacek V. Biogeochemical controls and feedbacks on ocean primary production. Science. 1998;281:200–207. PubMed

Tréguer P, et al. Influence of diatom diversity on the ocean biological carbon pump. Nature Geo. 2018;11:27.

Mann DG, Vanormelingen P. An inordinate fondness? The number, distributions, and origins of diatom species. J Eukaryot Microbiol. 2013;60:414–420. PubMed

Malviya S, et al. Insights into global diatom distribution and diversity in the world’s ocean. Proc Natl Acad Sci USA. 2016;113:1516–1525. PubMed PMC

Parks MB, Wickett NJ, Alverson AJ. Signal, uncertainty, and conflict in phylogenomic data for a diverse lineage of microbial eukaryotes (Diatoms, Bacillariophyta) Mol Biol Evol. 2017;35:80–93. PubMed PMC

Sorhannus U, Fox MG. Phylogenetic analyses of a combined data set suggest that the Attheya lineage is the closest living relative of the pennate diatoms (Bacillariophyceae) Protist. 2012;163:252–262. PubMed

Theriot EC, Ashworth M, Ruck E, Nakov T, Jansen RK. A preliminary multigene phylogeny of the diatoms (Bacillariophyta): challenges for future research. Plant Ecol Evol. 2010;143:278–296.

Gachon CMM, et al. The CCAP KnowledgeBase: linking protistan and cyanobacterial biological resources with taxonomic and molecular data. Systemat Biodiv. 2013;11:407–413.

Boundy-Mills K, et al. The United States Culture Collection Network (USCCN): Enhancing microbial genomics research through living microbe culture collections. Appl Environ Microbiol. 2015;81:5671–5674. PubMed PMC

Nanjappa D, Sanges R, Ferrante MI, Zingone A. Diatom flagellar genes and their expression during sexual reproduction in Leptocylindrus danicus. BMC Genomics. 2017;18:813. PubMed PMC

Nanjappa D, Audic S, Romac S, Kooistra WHCF, Zingone A. Assessment of species diversity and distribution of an ancient diatom lineage using a DNA metabarcoding approach. PLoS One. 2014;9:e103810. PubMed PMC

Nanjappa D, d’Ippolito G, Gallo C, Zingone A, Fontana A. Oxylipin diversity in the diatom family Leptocylindraceae reveals DHA derivatives in marine diatoms. Mar Drugs. 2014;12:368–384. PubMed PMC

Nanjappa D, Kooistra WHCF, Zingone A. A reappraisal of the genus Leptocylindrus (Bacillariophyta), with the addition of three species and the erection of Tenuicylindrus gen. nov. J Phycol. 2013;49:917–936. PubMed

Li CL, et al. Ultrastructural and molecular characterization of diversity among small araphid diatoms all lacking rimoportulae. I. Five new genera, eight new species. J Phycol. 2016;52:1018–1036. PubMed

Sato S, Matsumoto S, Medlin LK. Fine structure and 18S rDNA phylogeny of a marine araphid pennate diatom Plagiostriata goreensis gen. et sp nov (Bacillariophyta) Phycol Res. 2009;57:25–35.

Li CL, et al. The morphology and molecular phylogenetics of some marine diatom taxa within the Fragilariaceae, including twenty undescribed species and their relationship to Nanofrustulum. Opephora and Pseudostaurosira. Phytotaxa. 2018;355:1–104.

Medlin LK, Kooistra WHCF, Gersonde R, Wellbrock U. Evolution of the diatoms (Bacillariophyta). II. Nuclear-encoded small-subunit rRNA sequence comparisons confirm a paraphyletic origin for the centric diatoms. Mol Biol Evol. 1996;13:67–75. PubMed

Pickett-Heaps JD, McDonald KL, Tippit DH. Cell division in the pennate diatom Diatoma vulgare. Protoplasma. 1975;86:205–242. PubMed

Mayama S, Kuriyama A. Diversity of mineral cell coverings and their formation processes: a review focused on the siliceous cell coverings. J Plant Res. 2002;115:289–295. PubMed

F. E. Round, R. M. Crawford, D. G. Mann, Diatoms. Biology and morphology of the genera. Cambridge University Press. (1990)

Kang D, Froula J, Egan R, Wang Z. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ. 2015;3:e1165. PubMed PMC

Kazamia E, et al. Endocytosis-mediated siderophore uptake as a strategy for Fe acquisition in diatoms. Sci Adv. 2018;4:4536. PubMed PMC

Rastogi A, et al. Integrative analysis of large scale transcriptome data draws a comprehensive landscape of Phaeodactylum tricornutum genome and evolutionary origin of diatoms. Sci Rep. 2018;8:4834. PubMed PMC

Lommer M, et al. Genome and low-iron response of an oceanic diatom adapted to chronic iron limitation. Genome Biology. 2012;13:R66. PubMed PMC

Galachyants YP, et al. Sequencing of the complete genome of an araphid pennate diatom Synedra acus subsp. radians from Lake Baikal. Dokl Biochem Biophys. 2015;461:84–88. PubMed

Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31:3210–3212. PubMed

Dorrell RG, et al. Principles of plastid reductive evolution illuminated by nonphotosynthetic chrysophytes. Proc Natl Acad Sci USA. 2019;116:6914–6923. PubMed PMC

Bernardes JS, et al. Improvement in protein domain identification is reached by breaking consensus, with the agreement of many profiles and domain co-occurrence. PLoS Computational Biology. 2016;12(7):e1005038. PubMed PMC

http://current.geneontology.org/ontology/external2go/pfam2go

Bowler C, et al. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature. 2008;456:239. PubMed

Armbrust EV, et al. The genome of the diatom Thalassiosira pseudonana: Ecology, evolution, and metabolism. Science. 2004;306:79–86. PubMed

Mock T, et al. Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus. Nature. 2017;541:536–540. PubMed

Dorrell RG, et al. Chimeric origins of ochrophytes and haptophytes revealed through an ancient plastid proteome. Elife. 2017;6:23717. PubMed PMC

Méheust R, Zelzion E, Bhattacharya D, Lopez P, Bapteste E. Protein networks identify novel symbiogenetic genes resulting from plastid endosymbiosis. Proc Natl Acad Sci USA. 2016;113:3579–3584. PubMed PMC

Cooper MB, Smith AG. Exploring mutualistic interactions between microalgae and bacteria in the omics age. Curr Opin Plant Biol. 2015;26:147–153. PubMed

Newton RJ, et al. Genome characteristics of a generalist marine bacterial lineage. ISME J. 2010;4:784–798. PubMed

Wagner-Döbler I, et al. The complete genome sequence of the algal symbiont Dinoroseobacter shibae: a hitchhiker’s guide to life in the sea. ISME J. 2010;4:61–77. PubMed

Elifantz H, Horn G, Ayon M, Cohen Y, Minz D. Rhodobacteraceae are the key members of the microbial community of the initial biofilm formed in Eastern Mediterranean coastal seawater. FEMS Microbiol. Ecol. 2013;85:348–357. PubMed

Buchan A, LeCleir GR, Gulvik CA, González JM. Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat Rev Microbiol. 2014;12:686–698. PubMed

Muñoz-Gómez SA, et al. An updated phylogeny of the Alpha-proteobacteria reveals that the parasitic Rickettsiales and Holosporales have independent origins. Elife. 2019;8:42535. PubMed PMC

Keeling PJ, 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 PMC

Matasci, et al. Data access for the 1,000 Plants (1KP) project. Gigascience. 2014;3:17. PubMed PMC

Hahnke S, et al. Distinct seasonal growth patterns of the bacterium Planktotalea frisia in the North Sea and specific interaction with phytoplankton algae. FEMS Microbiol Ecol. 2013;86:185–199. PubMed

Henry CS, et al. High-throughput generation, optimization and analysis of genome-scale metabolic models. Nat Biotechnol. 2010;28:977–982. PubMed

Kazamia E, et al. Mutualistic interactions between vitamin B12‐dependent algae and heterotrophic bacteria exhibit regulation. Env microbiol. 2012;14.6:1466–1476. PubMed

Cooper MB, et al. Cross-exchange of B-vitamins underpins a mutualistic interaction between Ostreococcus tauri and Dinoroseobacter shibae. ISME J. 2019;13:334–345. PubMed PMC

Helliwell KE, Wheeler GL, Leptos KC, Goldstein RE, Smith AG. Insights into the evolution of vitamin B12 auxotrophy from sequenced algal genomes. Mol Biol Evol. 2011;28:2921–2933. PubMed

Helliwell KE, et al. Cyanobacteria and eukaryotic algae use different chemical variants of vitamin B12. Current Biology. 2016;26.8:999–1008. PubMed PMC

Amin SA, et al. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature. 2015;522:98–101. PubMed

Wienhausen G, Noriega-Ortega BE, Niggemann J, Dittmar T, Simon M. The exometabolome of two model strains of the the Roseobacter group: a marketplace of microbial metabolites. Front Microbiol. 2017;8:1985. PubMed PMC

Windler M, et al. Influence of bacteria on cell size development and morphology of cultivated diatoms. Phycol Res. 2014;62:13.

Lima-Mendez G, et al. Ocean plankton. Determinants of community structure in the global plankton interactome. Science. 2015;348:1262073. PubMed

Vincent FJ, et al. The epibiotic life of the cosmopolitan diatom Fragilariopsis doliolus on heterotrophic ciliates in the open ocean. ISME J. 2018;12:1094–1108. PubMed PMC

Ferrón S, Ho DT, Johnson ZI, Huntley ME. Air-water fluxes of N2O and CH4 during microalgae (Staurosira sp.) cultivation in an open raceway pond. Environ Sci Technol. 2012;46:10842–10848. PubMed

De Angelis R, et al. The diatom Staurosirella pinnata for photoactive material production. PLoS One. 2016;11:e0165571. PubMed PMC

Burge C, Karlin S. Prediction of complete gene structures in human genomic DNA. Journal of molecular biology. 1997;268:78–94. PubMed

Wang DM, et al. Nannochloropsis genomes reveal evolution of microalgal oleaginous traits. PLoS Genet. 2014;10:e1004094. PubMed PMC

Cock JM, et al. The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature. 2010;465:617–621. PubMed

Gobler CJ, et al. Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics. Proc Natl Acad Sci USA. 2011;108:4352–4357. PubMed PMC

Nishitsuji K, et al. A draft genome of the brown alga, Cladosiphon okamuranus, S-strain: a platform for future studies of ‘mozuku’ biology. DNA Res. 2016;23:10. PubMed PMC

Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–1313. PubMed PMC

Katoh K, Kuma K, Toh H, Miyata T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucl Acids Res. 2005;33:511–518. PubMed PMC

Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res. 2004;32:1792–1797. PubMed PMC

Kearse M, et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–1649. PubMed PMC

Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25:1972–1973. PubMed PMC

Tanaka T, et al. Oil accumulation by the oleaginous diatom Fistulifera solaris as revealed by the genome and transcriptome. The Plant Cell. 2015;27:162–176. PubMed PMC