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Paerl, RW, Bouget F-Y, Lozano J-C, Verge V, Schatt P, Allen EE, Palenik B, Azam F.  2016.  Use of plankton-derived vitamin B1 precursors, especially thiazole-related precursor, by key marine picoeukaryotic phytoplankton. ISME J. : The Author(s)   10.1038/ismej.2016.145   Abstract

Several cosmopolitan marine picoeukaryotic phytoplankton are B1 auxotrophs requiring exogenous vitamin B1 or precursor to survive. From genomic evidence, representatives of picoeukaryotic phytoplankton (Ostreococcus and Micromonas spp.) were predicted to use known thiazole and pyrimidine B1 precursors to meet their B1 demands, however, recent culture-based experiments could not confirm this assumption. We hypothesized these phytoplankton strains could grow on precursors alone, but required a thiazole-related precursor other the well-known and extensively tested 4-methyl-5-thiazoleethanol. This hypothesis was tested using bioassays and co-cultures of picoeukaryotic phytoplankton and bacteria. We found that specific B1-synthesizing proteobacteria and phytoplankton are sources of a yet-to-be chemically identified thiazole-related precursor(s) that, along with pyrimidine B1 precursor 4-amino-5-hydroxymethyl-2-methylpyrimidine, can support growth of Ostreococcus spp. (also Micromonas spp.) without B1. We additionally found that the B1-synthesizing plankton do not require contact with picoeukaryotic phytoplankton cells to produce thiazole-related precursor(s). Experiments with wild-type and genetically engineered Ostreococcus lines revealed that the thiazole kinase, ThiM, is required for growth on precursors, and that thiazole-related precursor(s) accumulate to appreciable levels in the euphotic ocean. Overall, our results point to thiazole-related B1 precursors as important micronutrients promoting the survival of abundant phytoplankton influencing surface ocean production and biogeochemical cycling.

Paerl, RW, Bertrand EM, Allen AE, Palenik B, Azam F.  2015.  Vitamin B1 ecophysiology of marine picoeukaryotic algae: Strain-specific differences and a new role for bacteria in vitamin cycling. Limnology and Oceanography. 60:215-228.   10.1002/lno.10009   AbstractWebsite

We confirmed multiple picoeukaryotic algae, Ostreococcus, Micromonas, and Pelagomonas spp., as thiamine (vitamin B1) auxotrophs in laboratory experiments with axenic cultures. Examined strains have half saturation growth constants (K-s) for B1 between 1.26 and 6.22 pmol B1 L-1, which is higher than reported seawater concentrations. Minimum B1 cell quotas for Ostreococcus and Micromonas spp. are high (2.20 x 10(-8)-4.46 x 10(-8) pmol B1 cell(-1)) relative to other B1 auxotrophic phytoplankton, potentially making them B1 rich prey for zooplankton and significant B1 reservoirs in oligotrophic marine habitats. Ostreococcus and Micromonas genomes are nonuniformly missing portions of the B1 biosynthesis pathway. Given their gene repertoires, Ostreococcus lucimarinus CCE9901 and Ostreococcus tauri OTH95 are expected to salvage B1 from externally provided 4-methyl-5-thiazoleethanol (HET) and 4-amino-5-hydroxymethyl-2-methylpyrimidine (HMP). However, in culture, neither could use HET plus HMP instead of B1, highlighting current limitations of genome-based prediction of B1 salvaging by picoeukaryotic algae. HMP and phosphorylated B1 use varied amongst tested strains and notably all Prasinophytes tested could not use HMP. B1-limited O. lucimarinus CCE9901 could not grow on added thiamine diphosphate (TDP), a phosophorylated B1 form. However, in co-culture with Pseudoalteromonas sp. TW7, a bacterium known to exhibit phosphatase activity, O. lucimarinus CCE9901 exhibited increased growth following TDP additions. This demonstrates that bacteria influence vitamin B1 availability beyond de novo synthesis and consumption; they can also serve as conduits that chemically alter, but not completely degrade or retain B1 analogs (e.g., TDP), and make them accessible to a broader range of microbes.

Palenik, B, Ren Q, Dupont CL, Myers GS, Heidelberg JF, Badger JH, Madupu R, Nelson WC, Brinkac LM, Dodson RJ, Durkin SA, Daugherty SC, Sullivan SA, Khouri H, Mohamoud Y, Halpin R, Paulsen IT.  2006.  Genome sequence of Synechococcus CC9311: Insights into adaptation to a coastal environment. Proceedings of the National Academy of Sciences of the United States of America. 103:13555-13559.   10.1073/pnas.0602963103   AbstractWebsite

Coastal aquatic environments are typically more highly productive and dynamic than open ocean ones. Despite these differences, cyanobacteria from the genus Synechococcus are important primary producers in both types of ecosystems. We have found that the genome of a coastal cyanobacterium, Synechococcus sp. strain CC9311, has significant differences from an open ocean strain, Synechococcus sp. strain WH8102, and these are consistent with the differences between their respective environments. CC9311 has a greater capacity to sense and respond to changes in its (coastal) environment. It has a much larger capacity to transport, store, use, or export metals, especially iron and copper. In contrast, phosphate acquisition seems less important, consistent with the higher concentration of phosphate in coastal environments. CC9311 is predicted to have differences in its outer membrane lipopolysaccharide, and this may be characteristic of the speciation of some cyanobacterial groups. In addition, the types of potentially horizontally transferred genes are markedly different between the coastal and open ocean genomes and suggest a more prominent role for phages in horizontal gene transfer in oligotrophic environments.

Palenik, B, Morel FMM.  1988.  Dark production of hydrogen peroxide in the Sargasso Sea. Limnology and Oceanography. 33:1606-1611. AbstractWebsite
Palenik, B.  2015.  Molecular mechanisms by which marine phytoplankton respond to their dynamic chemical environment. Annual Review of Marine Science, Vol 7. 7:325-340.   10.1146/annurev-marine-010814-015639   AbstractWebsite

Marine scientists have long been interested in the interactions of marine phytoplankton with their chemical environments. Nutrient availability clearly controls carbon fixation on a global scale, but the interactions between phytoplankton and nutrients are complex and include both short-term responses (seconds to minutes) and longer-term evolutionary adaptations. This review outlines how genomics and functional genomics approaches are providing a better understanding of these complex interactions, especially for cyanobacteria and diatoms, for which the genome sequences of multiple model organisms are available. Transporters and related genes are emerging as the most likely candidates for biomarkers in stress-specific studies, but other genes are also possible candidates. One surprise has been the important role of horizontal gene transfer in mediating chemical-biological interactions.

Palenik, B, Wood MA.  1998.  Molecular markers of phytoplankton status and their application at the level of individual cells. Molecular Approaches To The Study Of The Ocean. ( Cooksey KL, Ed.).:187-205., New York: Chapman & Hall Abstract
Palenik, B, Price NM, Morel FMM.  1991.  Potential effects of UV-B on the chemical environment of marine organisms . Environmental Pollution. 70:117-130.   10.1016/0269-7491(91)90084-a   AbstractWebsite

An increase in ultraviolet-B (UV-B) due to depletion of stratospheric ozone may affect growth of marine phytoplankton by altering the chemistry of their environment. Production of bioactive free radicals, photodecomposition of organic matter, and availability of trace metals are likely to be altered by increased UV-B flux. Such changes to the chemical environment may be both deleterious and benefical to marine phytoplankton. Extracellular free radicals such as OH, Br2-, and CO3- are predicted to have a negligible impact, but superoxide and its decomposition product hydrogen peroxide may react rapidly with cell surfaces and destroy membrane function and integrity. Increased UV-B will enhance the bioavailability of the redox active trace metals Fe and Cu. Thus, in the Fe-limited high latitude ocean, increased Fe availability may promote phytoplankton production, while in other parts of the ocean increased Cu availability may be toxic. Overall, the interdependent direct and indirect effects of UV-B on phytoplanton may compensate for each other and account for the ability of marine ecosystems to be subjected to widely variable UV-B flux without apparent damage.

Palenik, B, Henson SE.  1997.  The use of amides and other organic nitrogen sources by the phytoplankton Emiliania huxleyi. Limnology and Oceanography. 42:1544-1551. AbstractWebsite

Although dissolved organic nitrogen (DON) is beginning to be seen as a potentially important nitrogen source for phytoplankton, much remains to be learned about its components and their utilization. Emiliania huxleyi, a cosmopolitan eukaryotic phytoplankton species abundant in oligotrophic oceans and during blooms in some coastal regions, was screened for use of various DON compounds. Hypoxanthine and other purines support the nickel-dependent growth of most E. huxleyi strains. Acetamide and formamide but not longer chain aliphatic amides were found to be excellent nitrogen sources for growth; other phytoplankton were also found to utilize acetamide but not formamide. In E. huxleyi, small amides are transported into the cell followed by degradation to ammonia, possibly by amide-specific enzymes. The related molecules hydroxyurea and thiourea were toxic to the cells and caused an increase in fluorescence consistent with blockage of photosystem II. This fluorescence increase was inhibited by urea and acetamide, suggesting transport of hydroxyurea, thiourea, urea, and acetamide by the same or closely related transporters.

Palenik, B, Morel FMM.  1990.  Amino acid utilization by a marine phytoplankton: A novel mechanism. Limnology and Oceanography. 35:260-269. AbstractWebsite
Palenik, B, Grimwood J, Aerts A, Rouze P, Salamov A, Putnam N, Dupont C, Jorgensen R, Derelle E, Rombauts S, Zhou K, Otillar R, Merchant SS, Podell S, Gaasterland T, Napoli C, Gendler K, Manuell A, Tai V, Vallon O, Piganeau G, Jancek S, Heijde M, Jabbari K, Bowler C, Lohr M, Robbens S, Werner G, Dubchak I, Pazour GJ, Ren Q, Paulsen I, Delwiche C, Schmutz J, Rokhsar D, Van de Peer Y, Moreau H, Grigoriev IV.  2007.  The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proceedings of the National Academy of Sciences of the United States of America. 104:7705-7710.   10.1073/pnas.0611046104   AbstractWebsite

The smallest known eukaryotes, at approximate to 1-mu m diameter, are ostreococcus tauri and related species of marine phytoplankton. The genome of Ostreococcus lucimarinus has been completed and compared with that of O. tauri. This comparison reveals surprising differences across orthologous chromosomes in the two species from highly syntenic chromosomes in most cases to chromosomes with almost no similarity. Species divergence in these phytoplankton is occurring through multiple mechanisms acting differently on different chromosomes and likely including acquisition of new genes through horizontal gene transfer. We speculate that this latter process may be involved in altering the cell-surface characteristics of each species. In addition, the genome of O. lucimarinus provides insights into the unique metal metabolism of these organisms, which are predicted to have a large number of selenocysteine-containing proteins. Selenoenzymes are more catalytically active than similar enzymes lacking selenium, and thus the cell may require less of that protein. As reported here, selenoenzymes, novel fusion proteins, and loss of some major protein families including ones associated with chromatin are likely important adaptations for achieving a small cell size.

Palenik, B.  1994.  Cyanobacterial Community Structure as Seen from Rna-Polymerase Gene Sequence-Analysis. Applied and Environmental Microbiology. 60:3212-3219. AbstractWebsite

PCR was used to amplify DNA-dependent RNA polymerase gene sequences specifically from the cyanobacterial population in a seawater sample from the Sargasso Sea. Sequencing and analysis of the cloned fragments suggest that the population in the sample consisted of two distinct clusters of Prochlorococcus-like cyanobacteria and four clusters of Synechococcus-like cyanobacteria. The diversity within these clusters was significantly different, however. Clones within each Synechococcus-like cluster were 99 to 100% identical, while each Prochlorococcus-like cluster was only 91% identical at the nucleotide level. One Prochlorococcus-like cluster was significantly more closely related to a Mediterranean Sea (surface) Prochlorococcus isolate than to the other cluster, showing the highly divergent nature of this group even in one sample. The approach described here can be used as a general method for examining cyanobacterial diversity, while an oligotrophic ocean ecosystem such as the Sargasso Sea may be an ideal model for examining diversity in relation to environmental parameters.

Palenik, B, Block JC, Burns RG, Characklis WG, Christensen BE, Ghiorse WC, Gristina AG, Morel FMM, Nichols WW, Tuovinen OH, Tuschewitzki GJ, Videla HA.  1989.  Biofilms: Properties and processes. Structure and Function of Biofilms. 50( Characklis WG, Wilderer PA, Eds.).:351-366., Chichester: John Wiley & Sons, Ltd.   10.1002/jctb.280500315   Abstract
Palenik, B, Toledo G, Ferris M.  1999.  Cyanobacterial diversity in marine ecosystems as seen by RNA polymerase (rpoC1) gene sequences. Bulletin de l'Institut Oceanographique (Monaco). :101-105. AbstractWebsite
Palenik, B.  1992.  Polymerase evolution and organism evolution. Current opinion in genetics & development. 2:931-6.   10.1016/s0959-437x(05)80118-2   AbstractWebsite

The continuing exploration of the structure-function relationships of polymerases and the use of polymerases as phylogenetic tools complement each other, as seen in the literature for the past year. DNA-dependent RNA-polymerase gene sequences, in particular, have been used both to define functional domains in the protein encoded and recently to explore fundamental questions in evolution.

Palenik, B.  1998.  Why do isolates of eubacterial species have different growth rates under hte same conditions, in Microbial biosystems: new frontiers. 8th International Symposium on Microbial Ecology. ( Bell C, Brylinsky M, Johnson-Green PC, Eds.).:611-616., Halifax, Canada: Atlantic Canada Society for Microbial Ecology Abstract
Palenik, B, Morel FMM.  1990.  Comparison of cell-surface L-amino-acid oxidases from several marine-phytoplankton. Marine Ecology-Progress Series. 59:195-201.   10.3354/meps059195   AbstractWebsite
Palenik, B, Ren Q, Tai V, Paulsen IT.  2009.  Coastal Synechococcus metagenome reveals major roles for horizontal gene transfer and plasmids in population diversity. Environmental Microbiology. 11:349-359.   10.1111/j.1462-2920.2008.01772.x   AbstractWebsite

The extent to which cultured strains represent the genetic diversity of a population of microorganisms is poorly understood. Because they do not require culturing, metagenomic approaches have the potential to reveal the genetic diversity of the microbes actually present in an environment. From coastal California seawater, a complex and diverse environment, the marine cyanobacteria of the genus Synechococcus were enriched by flow cytometry-based sorting and the population metagenome was analysed with 454 sequencing technology. The sequence data were compared with model Synechococcus genomes, including those of two coastal strains, one isolated from the same and one from a very similar environment. The natural population metagenome had high sequence identity to most genes from the coastal model strains but diverged greatly from these genomes in multiple regions of atypical trinucleotide content that encoded diverse functions. These results can be explained by extensive horizontal gene transfer presumably with large differences in horizontally transferred genetic material between different strains. Some assembled contigs showed the presence of novel open reading frames not found in the model genomes, but these could not yet be unambiguously assigned to a Synechococcus clade. At least three distinct mobile DNA elements (plasmids) not found in model strain genomes were detected in the assembled contigs, suggesting for the first time their likely importance in marine cyanobacterial populations and possible role in horizontal gene transfer.

Palenik, B, Koke JA.  1995.  Characterization of a nitrogen-regulated protein identified by cell-surface biotinylation of a marine-phytoplankton. Applied and Environmental Microbiology. 61:3311-3315. AbstractWebsite

The biotinylating reagent succinimidyl 6-(biotinamido)hexanoate was used to label the cell surfaces of the cosmopolitan, marine, eukaryotic microorganism Emiliania huxleyi under different growth conditions. Proteins characteristic of different nutrient conditions could be identified. In particular, a nitrogen-regulated protein, nrp1, has an 82-kDa subunit that is present under nitrogen limitation and during growth on urea, It is absent under phosphate limitation or during exponential growth on nitrate or ammonia. nrp1 is the major membrane or wall protein in nitrogen-limited cells and is found in several strains of E, huxleyi, It may be a useful biomarker for examining the physiological state of E. huxleyi cells in their environment.

Palenik, B, Kieber DJ, Morel FMM.  1989.  Dissolved organic nitrogen use by phytoplankton: The role of cell-surface enzymes. Biological Oceanography. 6:347-354. AbstractWebsite
Palenik, B, Brahamsha B, Larimer FW, Land M, Hauser L, Chain P, Lamerdin J, Regala W, Allen EE, McCarren J, Paulsen I, Dufresne A, Partensky F, Webb EA, Waterbury J.  2003.  The genome of a motile marine Synechococcus. Nature. 424:1037.: Macmillan Magazines Ltd.   10.1038/nature01943   Abstract

Marine unicellular cyanobacteria are responsible for an estimated 20–40% of chlorophyll biomass and carbon fixation in the oceans1. Here we have sequenced and analysed the 2.4-megabase genome of Synechococcus sp. strain WH8102, revealing some of the ways that these organisms have adapted to their largely oligotrophic environment. WH8102 uses organic nitrogen and phosphorus sources and more sodium-dependent transporters than a model freshwater cyanobacterium. Furthermore, it seems to have adopted strategies for conserving limited iron stores by using nickel and cobalt in some enzymes, has reduced its regulatory machinery (consistent with the fact that the open ocean constitutes a far more constant and buffered environment than fresh water), and has evolved a unique type of swimming motility. The genome of WH8102 seems to have been greatly influenced by horizontal gene transfer, partially through phages. The genetic material contributed by horizontal gene transfer includes genes involved in the modification of the cell surface and in swimming motility. On the basis of its genome, WH8102 is more of a generalist than two related marine cyanobacteria2.

Palenik, B.  2001.  Chromatic adaptation in marine Synechococcus strains. Applied and Environmental Microbiology. 67:991-994.   10.1128/aem.67.2.991-994.2001   AbstractWebsite

Characterization of two genetically distinct groups of marine Synechococcus sp. strains shows that one, but not the other, increases its phycourobilin/phycoerythrobilin chromophore ratio when growing in blue light. This ability of at least some marine Synechococcus strains to chromatically adapt may help explain their greater abundance in particular ocean environments than cyanobacteria of the genus Prochlorococcus.

Palenik, B, Haselkorn R.  1992.  Multiple evolutionary origins of prochlorophytes, the chlorophyll b-containing prokaryotes. Nature. 355:265-267.   10.1038/355265a0   AbstractWebsite

PROCHLOROPHYTES are prokaryotes that Carry out oxygenic photosynthesis using chlorophylls a and b, but lack phycobiliproteins as light-harvesting pigments 1. These characteristics distinguish them from cyanobacteria, which contain phycobiliproteins, but no chlorophyll b. Three prochlorophyte genera have been described: Prochloron 1-3, Prochlorothrix 4 and Prochlorococcus 5,6. The prochlorophytes share their pigment characteristics with green plant and euglenoid chloroplasts, which has led to a debate on whether these chloroplasts may have arisen from an endosymbiotic prochlorophyte rather than a cyanobacterium 2,7. Molecular sequence data, including those presented here based on a fragment of the rpoC1 gene encoding a subunit of DNA-dependent RNA polymerase, indicate that the known prochlorophyte lineages do not include the direct ancestor of chloroplasts 8-11. We also show that the prochlorophytes are a highly diverged polyphyletic group. Thus the use of chlorophyll b as a light-harvesting pigment has developed independently several times in evolution. Similar conclusions have been reached in parallel studies using 16S ribosomal RNA sequences 12.

Palenik, B, Zafiriou OC, Morel FMM.  1987.  Hydrogen-peroxide production by a marine phytoplankton. Limnology and Oceanography. 32:1365-1369. AbstractWebsite
Palenik, B, Dyhrman ST.  1998.  Recent progress in understanding the regulation of marine primary productivity by phosphorus. Phosphorus in Plant Biology: Regulating Roles in Molecular, Cellular, Organismic and Ecosystem Processe. ( Lynch JP, Deikman J, Eds.).:26-38., Rockville, MD: American Society of Plant Physiologists Abstract
Palenik, B, Morel FMM.  1991.  Amine Oxidases of Marine-Phytoplankton. Applied and Environmental Microbiology. 57:2440-2443. AbstractWebsite

Some phytoplankton utilized a novel mechanism for obtaining nitrogen from primary amines. They oxidized the primary amines to produce extracellular hydrogen peroxide and aldehydes and used the third reaction product, ammonium, as a nitrogen source. The specificity, regulation, inhibition by bromoethylamine, and potential dependence on copper of this process are described.