Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics

Gobler, C J; Grigoriev, I V; Berry, D L; Dyhrman, S T; Wilhelm, S W; Salamov, A; Lobanov, A V; Zhang, Y; Collier, J L; Wurch, L L; Kustka, A B; Dill, B D; Shah, M; VerBerkomes, N C; Kuo, A; Terry, A; Pangilinan, J; Lindquist, E A; Lucas, S; Paulsen, I; Hattenrath-Lehmann, T K; Talmage, S; Walker, E A; Koch, F; Burson, A M; Marcoval, M A; Tang, Y; LeCleir, G R; Coyne, K J; Berg, G M; Bertrand, E M; Saito, M A; Gladyshev, V N

doi:10.1073/pnas.1016106108

Title: Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics

Journal Article · Wed Mar 02 00:00:00 EST 2011 · Proceedings of the National Academy of Sciences

DOI:https://doi.org/10.1073/pnas.1016106108· OSTI ID:1030219

Gobler, C J; Grigoriev, I V; Berry, D L; Dyhrman, S T; Wilhelm, S W; Salamov, A; Lobanov, A V; Zhang, Y; Collier, J L; Wurch, L L; Kustka, A B; Dill, B D; Shah, M; VerBerkomes, N C; Kuo, A; Terry, A; Pangilinan, J; Lindquist, E A; Lucas, S; Paulsen, I more »

Harmful algal blooms (HABs) cause significant economic and ecological damage worldwide. Despite considerable efforts, a comprehensive understanding of the factors that promote these blooms has been lacking because the biochemical pathways that facilitate their dominance relative to other phytoplankton within specific environments have not been identified. Here, biogeochemical measurements demonstrated that the harmful alga Aureococcus anophagefferens outcompeted co-occurring phytoplankton in estuaries with elevated levels of dissolved organic matter and turbidity and low levels of dissolved inorganic nitrogen. We subsequently sequenced the first HAB genome (A. anophagefferens) and compared its gene complement to those of six competing phytoplankton species identified via metaproteomics. Using an ecogenomic approach, we specifically focused on the gene sets that may facilitate dominance within the environmental conditions present during blooms. A. anophagefferens possesses a larger genome (56 mbp) and more genes involved in light harvesting, organic carbon and nitrogen utilization, and encoding selenium- and metal-requiring enzymes than competing phytoplankton. Genes for the synthesis of microbial deterrents likely permit the proliferation of this species with reduced mortality losses during blooms. Collectively, these findings suggest that anthropogenic activities resulting in elevated levels of turbidity, organic matter, and metals have opened a niche within coastal ecosystems that ideally suits the unique genetic capacity of A. anophagefferens and thus has facilitated the proliferation of this and potentially other HABs.

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Research Organization:: Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE

DOE Contract Number:: W-7405-ENG-48

OSTI ID:: 1030219

Report Number(s):: LLNL-JRNL-471739; TRN: US201124%%21

Journal Information:: Proceedings of the National Academy of Sciences, Journal Name: Proceedings of the National Academy of Sciences

Country of Publication:: United States

Language:: English

References (46)

Characterization of urease activity in three marine phytoplankton species, Aureococcus anophagefferens, Prorocentrum minimum, and Thalassiosira weissflogii Fan, C.; Glibert, P. M.; Alexander, J. Marine Biology, Vol. 142, Issue 5 https://doi.org/10.1007/s00227-003-1017-8	journal	February 2003
The ABC family of multidrug transporters in microorganisms van Veen, Hendrik W.; Konings, Wil N. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1365, Issue 1-2 https://doi.org/10.1016/S0005-2728(98)00039-5	journal	June 1998
Trace Metals and Dissolved Organic Carbon in an Estuary with Restricted River Flow and a Brown Tide Bloom Breuer, Eric; Sañudo-Wilhelmy, Sergio A.; Aller, Robert C. Estuaries, Vol. 22, Issue 3 https://doi.org/10.2307/1353048	journal	September 1999
CHARACTERIZATION AND EXPRESSION ANALYSIS OF THE Lhcf GENE FAMILY IN EMILIANIA HUXLEYI (HAPTOPHYTA) REVEALS DIFFERENTIAL RESPONSES TO LIGHT AND CO21: Lhcf GENE FAMILY IN EMILIANIA HUXLEYI Lefebvre, Stephane C.; Harris, Gayle; Webster, Richard Journal of Phycology, Vol. 46, Issue 1 https://doi.org/10.1111/j.1529-8817.2009.00793.x	journal	January 2010
Depletion, Degradation, and Recovery Potential of Estuaries and Coastal Seas Lotze, H. K. Science, Vol. 312, Issue 5781 https://doi.org/10.1126/science.1128035	journal	June 2006
ABC multidrug transporters: structure, function and role in chemoresistance Sharom, Frances J. Pharmacogenomics, Vol. 9, Issue 1 https://doi.org/10.2217/14622416.9.1.105	journal	January 2008
Signal transduction in the sexual life of Chlamydomonas Quarmby, Lynne M. Plant Molecular Biology, Vol. 26, Issue 5 https://doi.org/10.1007/BF00016474	journal	December 1994
The Genome of the Diatom Thalassiosira Pseudonana: Ecology, Evolution, and Metabolism Armbrust, E. V. Science, Vol. 306, Issue 5693 https://doi.org/10.1126/science.1101156	journal	October 2004
The Chlorophyll-Carotenoid Proteins of Oxygenic Photosynthesis Green, B. R.; Durnford, D. G. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 47, Issue 1 https://doi.org/10.1146/annurev.arplant.47.1.685	journal	June 1996
Correlated Evolution of Genome size and cell Volume in Diatoms (Bacillariophyceae) Connolly, Jessica A.; Oliver, Matthew J.; Beaulieu, Jeremy M. Journal of Phycology, Vol. 44, Issue 1 https://doi.org/10.1111/j.1529-8817.2007.00452.x	journal	February 2008
Trace Element Content of Selected Fertilizers and Dairy Manures as Determined by Icp–Ms McBride, Murray B.; Spiers, Graeme Communications in Soil Science and Plant Analysis, Vol. 32, Issue 1-2 https://doi.org/10.1081/CSS-100102999	journal	February 2001
A Transient Bloom of Ostreococcus (Chlorophyta, Prasinophyceae) in west neck bay, long Island, new york O'Kelly, Charles J.; Sieracki, Michael E.; Thier, Edward C. Journal of Phycology, Vol. 39, Issue 5 https://doi.org/10.1046/j.1529-8817.2003.02201.x	journal	September 2003
Nutrient-regulated transcriptional responses in the brown tide-forming alga Aureococcus anophagefferens: Aureococcus transcriptional response to N and P Wurch, Louie L.; Haley, Sheean T.; Orchard, Elizabeth D. Environmental Microbiology, Vol. 13, Issue 2 https://doi.org/10.1111/j.1462-2920.2010.02351.x	journal	September 2010
Positive Feedback and the Development and Persistence of Ecosystem Disruptive Algal Blooms Sunda, William G.; Graneli, Edna; Gobler, Christopher J. Journal of Phycology, Vol. 42, Issue 5 https://doi.org/10.1111/j.1529-8817.2006.00261.x	journal	October 2006
The evolutionary inheritance of elemental stoichiometry in marine phytoplankton Quigg, Antonietta; Finkel, Zoe V.; Irwin, Andrew J. Nature, Vol. 425, Issue 6955 https://doi.org/10.1038/nature01953	journal	September 2003
Harmful algal blooms: Their ecophysiology and general relevance to phytoplankton blooms in the sea Smayda, Theodore J. Limnology and Oceanography, Vol. 42, Issue 5part2 https://doi.org/10.4319/lo.1997.42.5_part_2.1137	journal	July 1997
Harmful algal blooms and eutrophication: Examining linkages from selected coastal regions of the United States Anderson, Donald M.; Burkholder, Joann M.; Cochlan, William P. Harmful Algae, Vol. 8, Issue 1 https://doi.org/10.1016/j.hal.2008.08.017	journal	December 2008
The Phaeodactylum genome reveals the evolutionary history of diatom genomes Bowler, Chris; Allen, Andrew E.; Badger, Jonathan H. Nature, Vol. 456, Issue 7219 https://doi.org/10.1038/nature07410	journal	October 2008
Comparative study of selenium requirements of three phytoplankton species: Gymnodinium catenatum, Alexandrium minutum (Dinophyta) and Chaetoceros cf. tenuissimus (Bacillariophyta) Doblin, M.; Blackburn, S.; Hallegraeff, G. Journal of Plankton Research, Vol. 21, Issue 6 https://doi.org/10.1093/plankt/21.6.1153	journal	June 1999
The Ectocarpus genome and the independent evolution of multicellularity in brown algae Cock, J. Mark; Sterck, Lieven; Rouzé, Pierre Nature, Vol. 465, Issue 7298 https://doi.org/10.1038/nature09016	journal	June 2010
Pico- and nanoplankton dynamics during bloom initiation of Aureococcus in a Long Island, NY bay Sieracki, Michael E.; Gobler, Christopher J.; Cucci, Terry L. Harmful Algae, Vol. 3, Issue 4 https://doi.org/10.1016/j.hal.2004.06.012	journal	November 2004
Extracellular phenoloxidase and peroxidase enzyme production during interspecific fungal interactions Score, Alan J.; Palfreyman, John W.; White, Nia A. International Biodeterioration & Biodegradation, Vol. 39, Issue 2-3 https://doi.org/10.1016/S0964-8305(97)00012-7	journal	January 1997
A Common Fold Mediates Vertebrate Defense and Bacterial Attack Rosado, C. J.; Buckle, A. M.; Law, R. H. P. Science, Vol. 317, Issue 5844 https://doi.org/10.1126/science.1144706	journal	August 2007
Ecosystem responses to internal and watershed organic matter loading:consequences for hypoxia in the eutrophying Neuse River Estuary, North Carolina, USA Paerl, Hw; Pinckney, Jl; Fear, Jm Marine Ecology Progress Series, Vol. 166 https://doi.org/10.3354/meps166017	journal	January 1998
How Selenium Has Altered Our Understanding of the Genetic Code Hatfield, Dolph L.; Gladyshev, Vadim N. Molecular and Cellular Biology, Vol. 22, Issue 11 https://doi.org/10.1128/MCB.22.11.3565-3576.2002	journal	June 2002
The ancient regulatory-protein family of WD-repeat proteins Neer, Eva J.; Schmidt, Carl J.; Nambudripad, Raman Nature, Vol. 371, Issue 6495 https://doi.org/10.1038/371297a0	journal	September 1994
Different Catalytic Mechanisms in Mammalian Selenocysteine- and Cysteine-Containing Methionine-R-Sulfoxide Reductases Kim, Hwa-Young; Gladyshev, Vadim N. PLoS Biology, Vol. 3, Issue 12 https://doi.org/10.1371/journal.pbio.0030375	journal	November 2005
The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003 Boeckmann, B. Nucleic Acids Research, Vol. 31, Issue 1 https://doi.org/10.1093/nar/gkg095	journal	January 2003
The Pfam protein families database Finn, Robert D.; Mistry, Jaina; Tate, John Nucleic Acids Research, Vol. 38, Issue suppl_1 https://doi.org/10.1093/nar/gkp985	journal	November 2009
Selenocysteine Stadtman, Thressa C. Annual Review of Biochemistry, Vol. 65, Issue 1 https://doi.org/10.1146/annurev.bi.65.070196.000503	journal	June 1996
A review of the causes, effects, and potential management of harmful brown tide blooms caused byAureococcus anophagefferens (Hargraves et sieburth) Gobler, C. J.; Lonsdale, D. J.; Boyer, G. L. Estuaries, Vol. 28, Issue 5 https://doi.org/10.1007/BF02732911	journal	October 2005
Genome sequence of Synechococcus CC9311: Insights into adaptation to a coastal environment Palenik, B.; Ren, Q.; Dupont, C. L. Proceedings of the National Academy of Sciences, Vol. 103, Issue 36 https://doi.org/10.1073/pnas.0602963103	journal	August 2006
The Alcaligenes eutrophus protein HoxN mediates nickel transport in Escherichia coli. Wolfram, L.; Friedrich, B.; Eitinger, T. Journal of bacteriology, Vol. 177, Issue 7 https://doi.org/10.1128/jb.177.7.1840-1843.1995	journal	January 1995
Sel1-like repeat proteins in signal transduction Mittl, Peer R. E.; Schneider-Brachert, Wulf Cellular Signalling, Vol. 19, Issue 1 https://doi.org/10.1016/j.cellsig.2006.05.034	journal	January 2007
Mediation of benthic–pelagic coupling by microphytobenthos: an energy- and material-based model for initiation of blooms of Aureococcus anophagefferens MacIntyre, Hugh L.; Lomas, Michael W.; Cornwell, Jeff Harmful Algae, Vol. 3, Issue 4 https://doi.org/10.1016/j.hal.2004.05.005	journal	November 2004
Selenium biogeochemistry in the San Francisco Bay estuary: changes in water column behavior Cutter, Gregory A.; Cutter, Lynda S. Estuarine, Coastal and Shelf Science, Vol. 61, Issue 3 https://doi.org/10.1016/j.ecss.2004.06.011	journal	November 2004
A LKALOID B IOSYNTHESIS IN P LANTS : Biochemistry, Cell Biology, Molecular Regulation, and Metabolic Engineering Applications Facchini, Peter J. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 52, Issue 1 https://doi.org/10.1146/annurev.arplant.52.1.29	journal	June 2001
The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation Palenik, B.; Grimwood, J.; Aerts, A. Proceedings of the National Academy of Sciences, Vol. 104, Issue 18 https://doi.org/10.1073/pnas.0611046104	journal	April 2007
New Light on the Scaling of Metabolic rate with the size of Algae Raven, John A.; Kubler, Janet E. Journal of Phycology, Vol. 38, Issue 1 https://doi.org/10.1046/j.1529-8817.2002.01125.x	journal	February 2002
Comparable levels of trace metal contamination in two semienclosed embayments: San Diego Bay and south San Francisco Bay Flegal, A. Russell; Sanudo-Wilhelmy, Sergio A. Environmental Science & Technology, Vol. 27, Issue 9 https://doi.org/10.1021/es00046a025	journal	September 1993
PHYSIOLOGICAL RESPONSES DURING DARK SURVIVAL AND RECOVERY IN AUREOCOCCUS ANOPHAGEFFERENS (PELAGOPHYCEAE) Popels, Linda C.; MacIntyre, Hugh L.; Warner, Mark E. Journal of Phycology, Vol. 43, Issue 1 https://doi.org/10.1111/j.1529-8817.2006.00303.x	journal	February 2007
Genome streamlining and the elemental costs of growth Hessen, Dag O.; Jeyasingh, Punidan D.; Neiman, Maurine Trends in Ecology & Evolution, Vol. 25, Issue 2 https://doi.org/10.1016/j.tree.2009.08.004	journal	February 2010
Evolutionary dynamics of eukaryotic selenoproteomes: large selenoproteomes may associate with aquatic life and small with terrestrial life Lobanov, Alexey V.; Fomenko, Dmitri E.; Zhang, Yan Genome Biology, Vol. 8, Issue 9 https://doi.org/10.1186/gb-2007-8-9-r198	journal	January 2007
A Phylogenetic Assessment of the Eukaryotic Light-Harvesting Antenna Proteins, with Implications for Plastid Evolution Durnford, D. G.; Deane, J. A.; Tan, S. Journal of Molecular Evolution, Vol. 48, Issue 1 https://doi.org/10.1007/PL00006445	journal	January 1999
Peptide hydrolysis, amino acid oxidation, and nitrogen uptake in communities seasonally dominated by Aureococcus anophagefferens Mulholland, Margaret R.; Gobler, Christopher J.; Lee, Cindy Limnology and Oceanography, Vol. 47, Issue 4 https://doi.org/10.4319/lo.2002.47.4.1094	journal	July 2002
Eutrophication and harmful algal blooms: A scientific consensus Heisler, J.; Glibert, P. M.; Burkholder, J. M. Harmful Algae, Vol. 8, Issue 1 https://doi.org/10.1016/j.hal.2008.08.006	journal	December 2008

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58 GEOSCIENCES
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ECONOMICS
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Title: Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics

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