Worden
Alexandra Z.
Worden
Alexandra Z.
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ArticleSeasonal and geographical transitions in eukaryotic phytoplankton community structure in the Atlantic and Pacific Oceans(Frontiers Media, 2020-09-30) Choi, Chang Jae ; Jimenez, Valeria ; Needham, David M. ; Poirier, Camille ; Bachy, Charles ; Alexander, Harriet ; Wilken, Susanne ; Chavez, Francisco P. ; Sudek, Sebastian ; Giovannoni, Stephen J. ; Worden, Alexandra Z.Much is known about how broad eukaryotic phytoplankton groups vary according to nutrient availability in marine ecosystems. However, genus- and species-level dynamics are generally unknown, although important given that adaptation and acclimation processes differentiate at these levels. We examined phytoplankton communities across seasonal cycles in the North Atlantic (BATS) and under different trophic conditions in the eastern North Pacific (ENP), using phylogenetic classification of plastid-encoded 16S rRNA amplicon sequence variants (ASVs) and other methodologies, including flow cytometric cell sorting. Prasinophytes dominated eukaryotic phytoplankton amplicons during the nutrient-rich deep-mixing winter period at BATS. During stratification (‘summer’) uncultured dictyochophytes formed ∼35 ± 10% of all surface plastid amplicons and dominated those from stramenopile algae, whereas diatoms showed only minor, ephemeral contributions over the entire year. Uncultured dictyochophytes also comprised a major fraction of plastid amplicons in the oligotrophic ENP. Phylogenetic reconstructions of near-full length 16S rRNA sequences established 11 uncultured Dictyochophyte Environmental Clades (DEC). DEC-I and DEC-VI dominated surface dictyochophytes under stratification at BATS and in the ENP, and DEC-IV was also important in the latter. Additionally, although less common at BATS, Florenciella-related clades (FC) were prominent at depth in the ENP. In both ecosystems, pelagophytes contributed notably at depth, with PEC-VIII (Pelagophyte Environmental Clade) and (cultured) Pelagomonas calceolata being most important. Q-PCR confirmed the near absence of P. calceolata at the surface of the same oligotrophic sites where it reached ∼1,500 18S rRNA gene copies ml–1 at the DCM. To further characterize phytoplankton present in our samples, we performed staining and at-sea single-cell sorting experiments. Sequencing results from these indicated several uncultured dictyochophyte clades are comprised of predatory mixotrophs. From an evolutionary perspective, these cells showed both conserved and unique features in the chloroplast genome. In ENP metatranscriptomes we observed high expression of multiple chloroplast genes as well as expression of a selfish element (group II intron) in the psaA gene. Comparative analyses across the Pacific and Atlantic sites support the conclusion that predatory dictyochophytes thrive under low nutrient conditions. The observations that several uncultured dictyochophyte lineages are seemingly capable of photosynthesis and predation, raises questions about potential shifts in phytoplankton trophic roles associated with seasonality and long-term ocean change.
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ArticleThe Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP) : illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing(Public Library of Science, 2014-06-24) Keeling, Patrick J. ; Burki, Fabien ; Wilcox, Heather M. ; Allam, Bassem ; Allen, Eric E. ; Amaral-Zettler, Linda A. ; Armbrust, E. Virginia ; Archibald, John M. ; Bharti, Arvind K. ; Bell, Callum J. ; Beszteri, Bank ; Bidle, Kay D. ; Cameron, Connor T. ; Campbell, Lisa ; Caron, David A. ; Cattolico, Rose Ann ; Collier, Jackie L. ; Coyne, Kathryn J. ; Davy, Simon K. ; Deschamps, Phillipe ; Dyhrman, Sonya T. ; Edvardsen, Bente ; Gates, Ruth D. ; Gobler, Christopher J. ; Greenwood, Spencer J. ; Guida, Stephanie M. ; Jacobi, Jennifer L. ; Jakobsen, Kjetill S. ; James, Erick R. ; Jenkins, Bethany D. ; John, Uwe ; Johnson, Matthew D. ; Juhl, Andrew R. ; Kamp, Anja ; Katz, Laura A. ; Kiene, Ronald P. ; Kudryavtsev, Alexander N. ; Leander, Brian S. ; Lin, Senjie ; Lovejoy, Connie ; Lynn, Denis ; Marchetti, Adrian ; McManus, George ; Nedelcu, Aurora M. ; Menden-Deuer, Susanne ; Miceli, Cristina ; Mock, Thomas ; Montresor, Marina ; Moran, Mary Ann ; Murray, Shauna A. ; Nadathur, Govind ; Nagai, Satoshi ; Ngam, Peter B. ; Palenik, Brian ; Pawlowski, Jan ; Petroni, Giulio ; Piganeau, Gwenael ; Posewitz, Matthew C. ; Rengefors, Karin ; Romano, Giovanna ; Rumpho, Mary E. ; Rynearson, Tatiana A. ; Schilling, Kelly B. ; Schroeder, Declan C. ; Simpson, Alastair G. B. ; Slamovits, Claudio H. ; Smith, David R. ; Smith, G. Jason ; Smith, Sarah R. ; Sosik, Heidi M. ; Stief, Peter ; Theriot, Edward ; Twary, Scott N. ; Umale, Pooja E. ; Vaulot, Daniel ; Wawrik, Boris ; Wheeler, Glen L. ; Wilson, William H. ; Xu, Yan ; Zingone, Adriana ; Worden, Alexandra Z.Microbial ecology is plagued by problems of an abstract nature. Cell sizes are so small and population sizes so large that both are virtually incomprehensible. Niches are so far from our everyday experience as to make their very definition elusive. Organisms that may be abundant and critical to our survival are little understood, seldom described and/or cultured, and sometimes yet to be even seen. One way to confront these problems is to use data of an even more abstract nature: molecular sequence data. Massive environmental nucleic acid sequencing, such as metagenomics or metatranscriptomics, promises functional analysis of microbial communities as a whole, without prior knowledge of which organisms are in the environment or exactly how they are interacting. But sequence-based ecological studies nearly always use a comparative approach, and that requires relevant reference sequences, which are an extremely limited resource when it comes to microbial eukaryotes. In practice, this means sequence databases need to be populated with enormous quantities of data for which we have some certainties about the source. Most important is the taxonomic identity of the organism from which a sequence is derived and as much functional identification of the encoded proteins as possible. In an ideal world, such information would be available as a large set of complete, well-curated, and annotated genomes for all the major organisms from the environment in question. Reality substantially diverges from this ideal, but at least for bacterial molecular ecology, there is a database consisting of thousands of complete genomes from a wide range of taxa, supplemented by a phylogeny-driven approach to diversifying genomics. For eukaryotes, the number of available genomes is far, far fewer, and we have relied much more heavily on random growth of sequence databases, raising the question as to whether this is fit for purpose.
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ArticleNewly discovered deep-branching marine plastid lineages are numerically rare but globally distributed(Elsevier, 2017-01-09) Choi, Chang Jae ; Bachy, Charles ; Spiro Jaeger, Gualtiero ; Poirier, Camille ; Sudek, Lisa ; Sarma, V. V. S. S. ; Mahadevan, Amala ; Giovannoni, Stephen J. ; Worden, Alexandra Z.Ocean surface warming is resulting in an expansion of stratified, low-nutrient environments, a process referred to as ocean desertification. A challenge for assessing the impact of these changes is the lack of robust baseline information on the biological communities that carry out marine photosynthesis. Phytoplankton perform half of global biological CO2 uptake, fuel marine food chains, and include diverse eukaryotic algae that have photosynthetic organelles (plastids) acquired through multiple evolutionary events. While amassing data from ocean ecosystems for the Baselines Initiative (6,177 near full-length 16S rRNA gene sequences and 9.4 million high-quality 16S V1-V2 amplicons) we identified two deep-branching plastid lineages based on 16S rRNA gene data. The two lineages have global distributions, but do not correspond to known phytoplankton. How the newly discovered phytoplankton lineages contribute to food chains and vertical carbon export to the deep sea remains unknown, but their prevalence in expanding, low nutrient surface waters suggests they will have a role in future oceans.
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ArticlePan genome of the phytoplankton Emiliania underpins its global distribution(Nature Publishing Group, 2013-07-10) Read, Betsy A. ; Kegel, Jessica ; Klute, Mary J. ; Kuo, Alan J. ; Lefebvre, Stephane C. ; Maumus, Florian ; Mayer, Christoph ; Miller, John ; Monier, Adam ; Salamov, Asaf ; Young, Jeremy ; Aguilar, Maria ; Claverie, Jean-Michel ; Frickenhaus, Stephan ; Gonzalez, Karina ; Herman, Emily K. ; Lin, Yao-Cheng ; Napier, Johnathan ; Ogata, Hiroyuki ; Sarno, Analissa F. ; Shmutz, Jeremy ; Schroeder, Declan C. ; de Vargas, Colomban ; Verret, Frederic ; von Dassow, Peter ; Valentin, Klaus ; Van de Peer, Yves ; Wheeler, Glen L. ; Emiliania huxleyi Annotation Consortium ; Dacks, Joel B. ; Delwiche, Charles F. ; Dyhrman, Sonya T. ; Glockne, Gernot ; Joh, Uwe ; Richards, Thomas ; Worden, Alexandra Z. ; Zhang, Xiaoyu ; Grigoriev, Igor V.Coccolithophores have influenced the global climate for over 200 million years1. These marine phytoplankton can account for 20 per cent of total carbon fixation in some systems2. They form blooms that can occupy hundreds of thousands of square kilometres and are distinguished by their elegantly sculpted calcium carbonate exoskeletons (coccoliths), rendering them visible from space3. Although coccolithophores export carbon in the form of organic matter and calcite to the sea floor, they also release CO2 in the calcification process. Hence, they have a complex influence on the carbon cycle, driving either CO2 production or uptake, sequestration and export to the deep ocean4. Here we report the first haptophyte reference genome, from the coccolithophore Emiliania huxleyi strain CCMP1516, and sequences from 13 additional isolates. Our analyses reveal a pan genome (core genes plus genes distributed variably between strains) probably supported by an atypical complement of repetitive sequence in the genome. Comparisons across strains demonstrate that E. huxleyi, which has long been considered a single species, harbours extensive genome variability reflected in different metabolic repertoires. Genome variability within this species complex seems to underpin its capacity both to thrive in habitats ranging from the equator to the subarctic and to form large-scale episodic blooms under a wide variety of environmental conditions.
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ArticleGenetic tool development in marine protists: emerging model organisms for experimental cell biology(Nature Research, 2020-04-06) Faktorová, Drahomíra ; Nisbet, R. Ellen R. ; Fernández Robledo, José A. ; Casacuberta, Elena ; Sudek, Lisa ; Allen, Andrew E. ; Ares, Manuel, Jr. ; Aresté, Cristina ; Balestreri, Cecilia ; Barbrook, Adrian C. ; Beardslee, Patrick ; Bender, Sara J. ; Booth, David S. ; Bouget, François-Yves ; Bowler, Chris ; Breglia, Susana A. ; Brownlee, Colin ; Burger, Gertraud ; Cerutti, Heriberto ; Cesaroni, Rachele ; Chiurillo, Miguel A. ; Clemente, Thomas ; Coles, Duncan B. ; Collier, Jackie L. ; Cooney, Elizabeth C. ; Coyne, Kathryn J. ; Docampo, Roberto ; Dupont, Christopher L. ; Edgcomb, Virginia P. ; Einarsso, Elin ; Elustondo, Pía A. ; Federici, Fernan ; Freire-Beneitez, Veronica ; Freyria, Nastasia J. ; Fukuda, Kodai ; García, Paulo A. ; Girguis, Peter R. ; Gomaa, Fatma ; Gornik, Sebastian G. ; Guo, Jian ; Hampl, Vladimír ; Hanawa, Yutaka ; Haro-Contreras, Esteban R. ; Hehenberger, Elisabeth ; Highfield, Andrea ; Hirakawa, Yoshihisa ; Hopes, Amanda ; Howe, Christopher J. ; Hu, Ian ; Ibañez, Jorge ; Irwin, Nicholas A. T. ; Ishii, Yuu ; Janowicz, Natalia Ewa ; Jones, Adam C. ; Kachale, Ambar ; Fujimura-Kamada, Konomi ; Kaur, Binnypreet ; Kaye, Jonathan Z. ; Kazana, Eleanna ; Keeling, Patrick J. ; King, Nicole ; Klobutcher, Lawrence A. ; Lander, Noelia ; Lassadi, Imen ; Li, Zhuhong ; Lin, Senjie ; Lozano, Jean-Claude ; Luan, Fulei ; Maruyama, Shinichiro ; Matute, Tamara ; Miceli, Cristina ; Minagawa, Jun ; Moosburner, Mark ; Najle, Sebastián R. ; Nanjappa, Deepak ; Nimmo, Isabel C. ; Noble, Luke ; Novák Vanclová, Anna M. G. ; Nowacki, Mariusz ; Nuñez, Isaac ; Pain, Arnab ; Piersanti, Angela ; Pucciarelli, Sandra ; Pyrih, Jan ; Rest, Joshua S. ; Rius, Mariana ; Robertson, Deborah ; Ruaud, Albane ; Ruiz-Trillo, Iñaki ; Sigg, Monika A. ; Silver, Pamela A. ; Slamovits, Claudio H. ; Smith, G. Jason ; Sprecher, Brittany N. ; Stern, Rowena ; Swart, Estienne C. ; Tsaousis, Anastasios D. ; Tsypin, Lev ; Turkewitz, Aaron ; Turnšek, Jernej ; Valach, Matus ; Vergé, Valérie ; von Dassow, Peter ; von der Haar, Tobias ; Waller, Ross F. ; Wang, Lu ; Wen, Xiaoxue ; Wheeler, Glen L. ; Woods, April ; Zhang, Huan ; Mock, Thomas ; Worden, Alexandra Z. ; Lukes, JuliusDiverse microbial ecosystems underpin life in the sea. Among these microbes are many unicellular eukaryotes that span the diversity of the eukaryotic tree of life. However, genetic tractability has been limited to a few species, which do not represent eukaryotic diversity or environmentally relevant taxa. Here, we report on the development of genetic tools in a range of protists primarily from marine environments. We present evidence for foreign DNA delivery and expression in 13 species never before transformed and for advancement of tools for eight other species, as well as potential reasons for why transformation of yet another 17 species tested was not achieved. Our resource in genetic manipulation will provide insights into the ancestral eukaryotic lifeforms, general eukaryote cell biology, protein diversification and the evolution of cellular pathways.
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ArticlePhytoplankton surveys in the Arctic Fram Strait demonstrate the tiny eukaryotic alga Micromonas and other picoprasinophytes contribute to deep sea export(MDPI, 2022-05-03) Bachy, Charles ; Sudek, Lisa ; Choi, Chang Jae ; Eckmann, Charlotte A. ; Nöthig, Eva-Maria ; Metfies, Katja ; Worden, Alexandra Z.Critical questions exist regarding the abundance and, especially, the export of picophytoplankton (≤2 µm diameter) in the Arctic. These organisms can dominate chlorophyll concentrations in Arctic regions, which are subject to rapid change. The picoeukaryotic prasinophyte Micromonas grows in polar environments and appears to constitute a large, but variable, proportion of the phytoplankton in these waters. Here, we analyze 81 samples from the upper 100 m of the water column from the Fram Strait collected over multiple years (2009–2015). We also analyze sediment trap samples to examine picophytoplankton contributions to export, using both 18S rRNA gene qPCR and V1-V2 16S rRNA Illumina amplicon sequencing to assess the Micromonas abundance within the broader diversity of photosynthetic eukaryotes based on the phylogenetic placement of plastid-derived 16S amplicons. The material sequenced from the sediment traps in July and September 2010 showed that 11.2 ± 12.4% of plastid-derived amplicons are from picoplanktonic prasinophyte algae and other green lineage (Viridiplantae) members. In the traps, Micromonas dominated (83.6 ± 21.3%) in terms of the overall relative abundance of Viridiplantae amplicons, specifically the species Micromonas polaris. Temporal variations in Micromonas abundances quantified by qPCR were also observed, with higher abundances in the late-July traps and deeper traps. In the photic zone samples, four prasinophyte classes were detected in the amplicon data, with Micromonas again being the dominant prasinophyte, based on the relative abundance (89.4 ± 8.0%), but with two species (M. polaris and M. commoda-like) present. The quantitative PCR assessments showed that the photic zone samples with higher Micromonas abundances (>1000 gene copies per mL) had significantly lower standing stocks of phosphate and nitrate, and a shallower average depth (20 m) than those with fewer Micromonas. This study shows that despite their size, prasinophyte picophytoplankton are exported to the deep sea, and that Micromonas is particularly important within this size fraction in Arctic marine ecosystems.
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ArticleGenomes from uncultivated Pelagiphages reveal multiple phylogenetic clades exhibiting extensive auxiliary metabolic genes and cross-family multigene transfers(American Society for Microbiology, 2022-08-16) Wittmers, Fabian ; Needham, David M. ; Hehenberger, Elisabeth ; Giovannoni, Stephen J. ; Worden, Alexandra Z.For the abundant marine Alphaproteobacterium Pelagibacter (SAR11), and other bacteria, phages are powerful forces of mortality. However, little is known about the most abundant Pelagiphages in nature, such as the widespread HTVC023P-type, which is currently represented by two cultured phages. Using viral metagenomic data sets and fluorescence-activated cell sorting, we recovered 80 complete, undescribed Podoviridae genomes that form 10 phylogenomically distinct clades (herein, named Clades I to X) related to the HTVC023P-type. These expanded the HTVC023P-type pan-genome by 15-fold and revealed 41 previously unknown auxiliary metabolic genes (AMGs) in this viral lineage. Numerous instances of partner-AMGs (colocated and involved in related functions) were observed, including partners in nucleotide metabolism, DNA hypermodification, and Curli biogenesis. The Type VIII secretion system (T8SS) responsible for Curli biogenesis was identified in nine genomes and expanded the repertoire of T8SS proteins reported thus far in viruses. Additionally, the identified T8SS gene cluster contained an iron-dependent regulator (FecR), as well as a histidine kinase and adenylate cyclase that can be implicated in T8SS function but are not within T8SS operons in bacteria. While T8SS are lacking in known Pelagibacter, they contribute to aggregation and biofilm formation in other bacteria. Phylogenetic reconstructions of partner-AMGs indicate derivation from cellular lineages with a more recent transfer between viral families. For example, homologs of all T8SS genes are present in syntenic regions of distant Myoviridae Pelagiphages, and they appear to have alphaproteobacterial origins with a later transfer between viral families. The results point to an unprecedented multipartner-AMG transfer between marine Myoviridae and Podoviridae. Together with the expansion of known metabolic functions, our studies provide new prospects for understanding the ecology and evolution of marine phages and their hosts.