Publications

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Book Chapter
Morel, FMM, Palenik B.  1989.  The aquatic chemistry of biofilms. Structure and Function of Biofilms. 50( Characklis WG, Wilderer PA, Eds.).:351-366., Chichester: John Wiley & Sons, Ltd.   10.1002/jctb.280500315   Abstract
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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
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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
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Journal Article
Chisholm, SW, Frankel SL, Goericke R, Olson RJ, Palenik B, Waterbury JB, Westjohnsrud L, Zettler ER.  1992.  Prochlorococcus marinus nov. gen. nov. sp.: An oxyphototrophic marine prokaryote containing divinyl chlorophyll a and b . Archives of Microbiology. 157:297-300.   10.1007/bf00245165   AbstractWebsite

Several years ago, prochlorophyte picoplankton were discovered in the N. Atlantic. They have since been found to be abundant within the euphotic zone of the world's tropical and temperate oceans. The cells are extremely small, lack phycobiliproteins. and contain divinyl chlorophyll a and b as their primary photosynthetic pigments. Phylogenies constructed from DNA sequence data indicate that these cells are more closely related to a cluster of marine cyanobacteria than to their prochlorophyte 'relatives' Prochlorothrix and Prochloron. Several strains of this organism have recently been brought into culture, and herewith are given the name Prochlorococcus marinus.

Worden, AZ, Nolan JK, Palenik B.  2004.  Assessing the dynamics and ecology of marine picophytoplankton: The importance of the eukaryotic component. Limnology and Oceanography. 49:168-179. AbstractWebsite
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Taton, A, Unglaub F, Wright NE, Zeng WY, Paz-Yepes J, Brahamsha B, Palenik B, Peterson TC, Haerizadeh F, Golden SS, Golden JW.  2014.  Broad-host-range vector system for synthetic biology and biotechnology in cyanobacteria. Nucleic Acids Research. 42   10.1093/nar/gku673   AbstractWebsite

Inspired by the developments of synthetic biology and the need for improved genetic tools to exploit cyanobacteria for the production of renewable bio-products, we developed a versatile platform for the construction of broad-host-range vector systems. This platform includes the following features: (i) an efficient assembly strategy in which modules released from 3 to 4 donor plasmids or produced by polymerase chain reaction are assembled by isothermal assembly guided by short GC-rich overlap sequences. (ii) A growing library of molecular devices categorized in three major groups: (a) replication and chromosomal integration; (b) antibiotic resistance; (c) functional modules. These modules can be assembled in different combinations to construct a variety of autonomously replicating plasmids and suicide plasmids for gene knockout and knockin. (iii) A web service, the CYANO-VECTOR assembly portal, which was built to organize the various modules, facilitate the in silico construction of plasmids, and encourage the use of this system. This work also resulted in the construction of an improved broad-host-range replicon derived from RSF1010, which replicates in several phylogenetically distinct strains including a new experimental model strain Synechocystis sp. WHSyn, and the characterization of nine antibiotic cassettes, four reporter genes, four promoters, and a ribozyme-based insulator in several diverse cyanobacterial strains.

Wang, SY, Shi XG, Palenik B.  2016.  Characterization of Picochlorum sp use of wastewater generated from hydrothermal liquefaction as a nitrogen source. Algal Research-Biomass Biofuels and Bioproducts. 13:311-317.   10.1016/j.algal.2015.11.015   AbstractWebsite

Picochlorumsp. strain SENEW3 is a halotolerant green algawith high growth rates and the ability to utilize organic nitrogen sources including wastewater generated from hydrothermal liquefaction (HTL-WW). Picochlorum acclimates to the presence of HTL-WW. In a photosynthesis/respiration rate test, Picochlorum SENEW3 showed a stress response to HTL-WW additions in a dose-dependent manner while cells pre-grown with HTL-WW had a greatly reduced response to additions. A quantitative proteomics tool, iTRAQ, was applied to assess Picochlorum global proteome changes in response to HTL-WWas a nitrogen source. From this approach, a total of 350 different proteins were identified across 2 biological replicates which were significantly up-regulated or down-regulated (average ratio of more than 1.2 or less than 0.8, at least one p-value of <0.05). Protease and oxidative stress enzymes were notably up-regulated. An aminopeptidase enzyme assay showed that, compared to controls, cells grown with 0.1% (vol) HTL-WW had 2.1-fold higher protease activity. An ascorbate peroxidase assay showed an 8.6-fold increase in exponential cells grown with 0.1% HTL-WW compared to controls. This study provides insights into the development of microalgae for algal biofuel production using HTL wastewater recycling [1]. (C) 2015 Elsevier B.V. All rights reserved.

Su, ZC, Mao FL, Dam P, Wu HW, Olman V, Paulsen IT, Palenik B, Xu Y.  2006.  Computational inference and experimental validation of the nitrogen assimilation regulatory network in cyanobacterium Synechococcus sp WH 8102. Nucleic Acids Research. 34:1050-1065.   10.1093/nar/gkj496   AbstractWebsite

Deciphering the regulatory networks encoded in the genome of an organism represents one of the most interesting and challenging tasks in the post-genome sequencing era. As an example of this problem, we have predicted a detailed model for the nitrogen assimilation network in cyanobacterium Synechococcus sp. WH 8102 (WH8102) using a computational protocol based on comparative genomics analysis and mining experimental data from related organisms that are relatively well studied. This computational model is in excellent agreement with the microarray gene expression data collected under ammonium-rich versus nitrate-rich growth conditions, suggesting that our computational protocol is capable of predicting biological pathways/networks with high accuracy. We then refined the computational model using the microarray data, and proposed a new model for the nitrogen assimilation network in WH8102. An intriguing discovery from this study is that nitrogen assimilation affects the expression of many genes involved in photosynthesis, suggesting a tight coordination between nitrogen assimilation and photosynthesis processes. Moreover, for some of these genes, this coordination is probably mediated by NtcA through the canonical NtcA promoters in their regulatory regions.

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.

Armbrust, EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou SG, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, Jenkins BD, Jurka J, Kapitonov VV, Kroger N, Lau WWY, Lane TW, Larimer FW, Lippmeier JC, Lucas S, Medina M, Montsant A, Obornik M, Parker MS, Palenik B, Pazour GJ, Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatrakoln K, Valentin K, Vardi A, Wilkerson FP, Rokhsar DS.  2004.  The genome of the diatom Thalassiosira pseudonana: Ecology, evolution, and metabolism. Science. 306:79-86.   10.1126/science.1101156   AbstractWebsite

Diatoms are unicellular algae with plastids acquired by secondary endosymbiosis. They are responsible for similar to20% of global carbon fixation. We report the 34 million-base pair draft nuclear genome of the marine diatom Thalassiosira pseudonana and its 129 thousand-base pair ptastid and 44 thousand-base pair mitochondrial genomes. Sequence and optical restriction mapping revealed 24 diploid nuclear chromosomes. We identified novel genes for silicic acid transport and formation of silica-based cell walls, high-affinity iron uptake, biosynthetic enzymes for several types of polyunsaturated fatty acids, use of a range of nitrogenous compounds, and a complete urea cycle, all attributes that allow diatoms to prosper in aquatic environments.

Foflonker, F, Price DC, Qiu H, Palenik B, Wang SY, Bhattacharya D.  2015.  Genome of the halotolerant green alga Picochlorum sp reveals strategies for thriving under fluctuating environmental conditions. Environmental Microbiology. 17:412-426.   10.1111/1462-2920.12541   AbstractWebsite

An expected outcome of climate change is intensification of the global water cycle, which magnifies surface water fluxes, and consequently alters salinity patterns. It is therefore important to understand the adaptations and limits of microalgae to survive changing salinities. To this end, we sequenced the 13.5Mbp genome of the halotolerant green alga PicochlorumSENEW3 (SE3) that was isolated from a brackish water pond subject to large seasonal salinity fluctuations. PicochlorumSE3 encodes 7367 genes, making it one of the smallest and most gene dense eukaryotic genomes known. Comparison with the pico-prasinophyte Ostreococcus tauri, a species with a limited range of salt tolerance, reveals the enrichment of transporters putatively involved in the salt stress response in PicochlorumSE3. Analysis of cultures and the protein complement highlight the metabolic flexibility of PicochlorumSE3 that encodes genes involved in urea metabolism, acetate assimilation and fermentation, acetoin production and glucose uptake, many of which form functional gene clusters. Twenty-four cases of horizontal gene transfer from bacterial sources were found in PicochlorumSE3 with these genes involved in stress adaptation including osmolyte production and growth promotion. Our results identify PicochlorumSE3 as a model for understanding microalgal adaptation to stressful, fluctuating environments.

Dupont, CL, McCrow JP, Valas R, Moustafa A, Walworth N, Goodenough U, Roth R, Hogle SL, Bai J, Johnson ZI, Mann E, Palenik B, Barbeau KA, Craig Venter J, Allen AE.  2015.  Genomes and gene expression across light and productivity gradients in eastern subtropical Pacific microbial communities. ISME J. 9:1076-1092.: International Society for Microbial Ecology   10.1038/ismej.2014.198   Abstract

Transitions in community genomic features and biogeochemical processes were examined in surface and subsurface chlorophyll maximum (SCM) microbial communities across a trophic gradient from mesotrophic waters near San Diego, California to the oligotrophic Pacific. Transect end points contrasted in thermocline depth, rates of nitrogen and CO2 uptake, new production and SCM light intensity. Relative to surface waters, bacterial SCM communities displayed greater genetic diversity and enrichment in putative sulfur oxidizers, multiple actinomycetes, low-light-adapted Prochlorococcus and cell-associated viruses. Metagenomic coverage was not correlated with transcriptional activity for several key taxa within Bacteria. Low-light-adapted Prochlorococcus, Synechococcus, and low abundance gamma-proteobacteria enriched in the>3.0-[mu]m size fraction contributed disproportionally to global transcription. The abundance of these groups also correlated with community functions, such as primary production or nitrate uptake. In contrast, many of the most abundant bacterioplankton, including SAR11, SAR86, SAR112 and high-light-adapted Prochlorococcus, exhibited low levels of transcriptional activity and were uncorrelated with rate processes. Eukaryotes such as Haptophytes and non-photosynthetic Aveolates were prevalent in surface samples while Mamielles and Pelagophytes dominated the SCM. Metatranscriptomes generated with ribosomal RNA-depleted mRNA (total mRNA) coupled to in vitro polyadenylation compared with polyA-enriched mRNA revealed a trade-off in detection eukaryotic organelle and eukaryotic nuclear origin transcripts, respectively. Gene expression profiles of SCM eukaryote populations, highly similar in sequence identity to the model pelagophyte Pelagomonas sp. CCMP1756, suggest that pelagophytes are responsible for a majority of nitrate assimilation within the SCM.

Keeling, PJ, Burki F, Wilcox HM, Allam B, Allen EE, Amaral-Zettler LA, Armbrust VE, Archibald JM, Bharti AK, Bell CJ, Beszteri B, Bidle KD, Cameron CT, Campbell L, Caron DA, Cattolico RA, Collier JL, Coyne K, Davy SK, Deschamps P, Dyhrman ST, Edvardsen B, Gates RD, Gobler CJ, Greenwood SJ, Guida SM, Jacobi JL, Jakobsen KS, James ER, Jenkins B, John U, Johnson MD, Juhl AR, Kamp A, Katz LA, Kiene R, Kudryavtsev A, Leander BS, Lin S, Lovejoy C, Lynn D, Marchetti A, McManus G, Nedelcu AM, Menden-Deuer S, Miceli C, Mock T, Montresor M, Moran MA, Murray S, Nadathur G, Nagai S, Ngam PB, Palenik B, Pawlowski J, Petroni G, Piganeau G, Posewitz MC, Rengefors K, Romano G, Rumpho ME, Rynearson T, Schilling KB, Schroeder DC, Simpson AGB, Slamovits CH, Smith DR, Smith JG, Smith SR, Sosik HM, Stief P, Theriot E, Twary SN, Umale PE, Vaulot D, Wawrik B, Wheeler GL, Wilson WH, Xu Y, Zingone A, Worden AZ.  2014.  The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): Illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biol. 12:e1001889.: Public Library of Science   10.1371/journal.pbio.1001889   AbstractWebsite

Current sampling of genomic sequence data from eukaryotes is relatively poor, biased, and inadequate to address important questions about their biology, evolution, and ecology; this Community Page describes a resource of 700 transcriptomes from marine microbial eukaryotes to help understand their role in the world's oceans.

Sandhage, KH, Allan SM, Dickerson MB, Gaddis CS, Shian S, Weatherspoon MR, Cai Y, Ahmad G, Haluska MS, Snyder RL, Unocic RR, Zalar FM, Zhang YS, Rapp RA, Hildebrand M, Palenik BP.  2005.  Merging biological self-assembly with synthetic chemical tailoring: The potential for 3-D genetically engineered micro/nano-devices (3-D GEMS). International Journal of Applied Ceramic Technology. 2:317-326.   10.1111/j.1744-7402.2005.02035.x   AbstractWebsite

Appreciable global efforts are underway to develop processes for fabricating three-dimensional (3-D) nanostructured assemblies for advanced devices. Widespread commercialization of such devices will require: (i) precise 3-D fabrication of chemically tailored structures on a fine scale and (ii) mass production of such structures on a large scale. These often-conflicting demands can be addressed with a revolutionary new paradigm that couples biological self-assembly with synthetic chemistry: Bioclastic and Shape-preserving Inorganic Conversion (BaSIC). Nature provides numerous examples of microorganisms that assemble biominerals into intricate 3-D structures. Among the most spectacular of these microorganisms are diatoms (unicellular algae). Each of the tens of thousands of diatom species assembles silica nanoparticles into a microshell with a distinct 3-D shape and pattern of fine (nanoscale) features. The repeated doubling associated with biological reproduction enables enormous numbers of such 3-D microshells to be generated (e.g., only 40 reproduction cycles can yield >1 trillion 3-D replicas!). Such generic precision and massive parallelism are highly attractive for device manufacturing. However, the natural chemistries assembled by diatoms (and other microorganisms) are rather limited. With BaSIC processes, biogenic assemblies can be converted into a wide variety of new functional chemistries, while preserving the 3-D morphologies. Ongoing advances in genetic engineering promise to yield microorganisms tailored to assemble nanoparticle structures with device-specific shapes. Large-scale culturing of such genetically tailored microorganisms, coupled with shape-preserving chemical conversion (via BaSIC processes), would then provide low-cost 3-D Genetically Engineered Micro/nano-devices (3-D GEMs).

Wang, SY, Lambert W, Giang S, Goericke R, Palenik B.  2014.  Microalgal assemblages in a poikilohaline pond. Journal of Phycology. 50:303-309.   10.1111/jpy.12158   AbstractWebsite

Microalgal strains for algal biofuels production in outdoor ponds will need to have high net growth rates under diverse environmental conditions. A small, variable salinity pond in the San Elijo Lagoon estuary in southern California was chosen to serve as a model pond due to its routinely high chlorophyll content. Profiles of microalgal assemblages from water samples collected from April 2011 to January 2012 were obtained by constructing 18S rDNA environmental clone libraries. Pond assemblages were found to be dominated by green algae Picochlorum sp. and Picocystis sp. throughout the year. Pigment analysis suggested that the two species contributed most of the chlorophyll a of the pond, which ranged from 21.9 to 664.3 mu g center dot L-1 with the Picocystis contribution increasing at higher salinities. However, changes of temperature, salinity or irradiance may have enabled a bloom of the diatom Chaetoceros sp. in June 2011. Isolates of these microalgae were obtained and their growth rates characterized as a function of temperature and salinity. Chaetoceros sp. had the highest growth rate over the temperature test range while it showed the most sensitivity to high salinity. All three strains showed the presence of lipid bodies during nitrogen starvation, suggesting they have potential as future biofuels strains.

Bradley, JM, Svistunenko DA, Pullin J, Hill N, Stuart RK, Palenik B, Wilson MT, Hemmings AM, Moore GR, Le Brun NE.  2019.  Reaction of O-2 with a diiron protein generates a mixed-valent Fe2+/Fe3+ center and peroxide. Proceedings of the National Academy of Sciences of the United States of America. 116:2058-2067.   10.1073/pnas.1809913116   AbstractWebsite

The gene encoding the cyanobacterial ferritin SynFtn is up-regulated in response to copper stress. Here, we show that, while SynFtn does not interact directly with copper, it is highly unusual in several ways. First, its catalytic diiron ferroxidase center is unlike those of all other characterized prokaryotic ferritins and instead resembles an animal H-chain ferritin center. Second, as demonstrated by kinetic, spectro-scopic, and high-resolution X-ray crystallographic data, reaction of O-2 with the di-Fe2+ center results in a direct, one-electron oxidation to a mixed-valent Fe2+/Fe3+ form. Iron-O-2 chemistry of this type is currently unknown among the growing family of proteins that bind a diiron site within a four alpha-helical bundle in general and ferritins in particular. The mixed-valent form, which slowly oxidized to the more usual di-Fe3+ form, is an intermediate that is continually generated during mineralization. Peroxide, rather than superoxide, is shown to be the product of O-2 reduction, implying that ferroxidase centers function in pairs via long-range electron transfer through the protein resulting in reduction of O-2 bound at only one of the centers. We show that electron transfer is mediated by the transient formation of a radical on Tyr40, which lies similar to 4 angstrom from the diiron center. As well as demonstrating an expansion of the iron-O-2 chemistry known to occur in nature, these data are also highly relevant to the question of whether all ferritins mineralize iron via a common mechanism, providing unequivocal proof that they do not.

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.

Dufresne, A, Ostrowski M, Scanlan DJ, Garczarek L, Mazard S, Palenik BP, Paulsen IT, de Marsac NT, Wincker P, Dossat C, Ferriera S, Johnson J, Post AF, Hess WR, Partensky F.  2008.  Unraveling the genomic mosaic of a ubiquitous genus of marine cyanobacteria. Genome Biology. 9   10.1186/gb-2008-9-5-r90   AbstractWebsite

Background: The picocyanobacterial genus Synechococcus occurs over wide oceanic expanses, having colonized most available niches in the photic zone. Large scale distribution patterns of the different Synechococcus clades (based on 16S rRNA gene markers) suggest the occurrence of two major lifestyles ('opportunists'/'specialists'), corresponding to two distinct broad habitats ('coastal'/'open ocean'). Yet, the genetic basis of niche partitioning is still poorly understood in this ecologically important group. Results: Here, we compare the genomes of 11 marine Synechococcus isolates, representing 10 distinct lineages. Phylogenies inferred from the core genome allowed us to refine the taxonomic relationships between clades by revealing a clear dichotomy within the main subcluster, reminiscent of the two aforementioned lifestyles. Genome size is strongly correlated with the cumulative lengths of hypervariable regions (or 'islands'). One of these, encompassing most genes encoding the light-harvesting phycobilisome rod complexes, is involved in adaptation to changes in light quality and has clearly been transferred between members of different Synechococcus lineages. Furthermore, we observed that two strains (RS9917 and WH5701) that have similar pigmentation and physiology have an unusually high number of genes in common, given their phylogenetic distance. Conclusion: We propose that while members of a given marine Synechococcus lineage may have the same broad geographical distribution, local niche occupancy is facilitated by lateral gene transfers, a process in which genomic islands play a key role as a repository for transferred genes. Our work also highlights the need for developing picocyanobacterial systematics based on genome-derived parameters combined with ecological and physiological data.