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Palenik, B, Swift H.  1996.  Cyanobacterial evolution and prochlorophyte diversity as seen in DNA-dependent RNA polymerase gene sequences. Journal of Phycology. 32:638-646.   Doi 10.1111/J.0022-3646.1996.00638.X   AbstractWebsite

Nucleotide sequence data from DNA-dependent RNA polymerase (rpoC) genes were used to examine the phylogenetic relationships among the phycobiliprotein- and three known chlorophyll b-containing (prochlorophyte) cyanobacteria. The phylogenetic trees obtained confirm the polyphyletic nature of the prochlorophytes. Data from Prochloron cells obtained form six different tunicate host species suggest that at least two closely related groups of Prochloron exist in the same area in Palau, West Caroline Islands. Overall, however, the genetic diversity within the analyzed samples was much smaller than within the nonsymbiotic Prochlorococcus.

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
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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.

Stuart, RK, Bundy R, Buck K, Ghassemain M, Barbeau K, Palenik B.  2017.  Copper toxicity response influences mesotrophic Synechococcus community structure. Environmental Microbiology. 19:756-769.   10.1111/1462-2920.13630   AbstractWebsite

Picocyanobacteria from the genus Synechococcus are ubiquitous in ocean waters. Their phylogenetic and genomic diversity suggests ecological niche differentiation, but the selective forces influencing this are not well defined. Marine picocyanobacteria are sensitive to Cu toxicity, so adaptations to this stress could represent a selective force within, and between, species', also known as clades. Here, we compared Cu stress responses in cultures and natural populations of marine Synechococcus from two co-occurring major mesotrophic clades (I and IV). Using custom microarrays and proteomics to characterize expression responses to Cu in the lab and field, we found evidence for a general stress regulon in marine Synechococcus. However, the two clades also exhibited distinct responses to copper. The Clade I representative induced expression of genomic island genes in cultures and Southern California Bight populations, while the Clade IV representative downregulated Fe-limitation proteins. Copper incubation experiments suggest that Clade IV populations may harbour stress-tolerant subgroups, and thus fitness tradeoffs may govern Cu-tolerant strain distributions. This work demonstrates that Synechococcus has distinct adaptive strategies to deal with Cu toxicity at both the clade and subclade level, implying that metal toxicity and stress response adaptations represent an important selective force for influencing diversity within marine Synechococcus populations.

Mao, X, Olman V, Stuart R, Paulsen IT, Palenik B, Xu Y.  2010.  Computational prediction of the osmoregulation network in Synechococcus sp. WH8102. Bmc Genomics. 11   10.1186/1471-2164-11-291   AbstractWebsite

Background: Osmotic stress is caused by sudden changes in the impermeable solute concentration around a cell, which induces instantaneous water flow in or out of the cell to balance the concentration. Very little is known about the detailed response mechanism to osmotic stress in marine Synechococcus, one of the major oxygenic phototrophic cyanobacterial genera that contribute greatly to the global CO(2) fixation. Results: We present here a computational study of the osmoregulation network in response to hyperosmotic stress of Synechococcus sp strain WH8102 using comparative genome analyses and computational prediction. In this study, we identified the key transporters, synthetases, signal sensor proteins and transcriptional regulator proteins, and found experimentally that of these proteins, 15 genes showed significantly changed expression levels under a mild hyperosmotic stress. Conclusions: From the predicted network model, we have made a number of interesting observations about WH8102. Specifically, we found that (i) the organism likely uses glycine betaine as the major osmolyte, and others such as glucosylglycerol, glucosylglycerate, trehalose, sucrose and arginine as the minor osmolytes, making it efficient and adaptable to its changing environment; and (ii) sigma(38), one of the seven types of sigma factors, probably serves as a global regulator coordinating the osmoregulation network and the other relevant networks.

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.

Xia, XM, Vidyarathna NK, Palenik B, Lee P, Liu HB.  2015.  Comparison of the seasonal variations of synechococcus assemblage structures in estuarine waters and coastal waters of Hong Kong. Applied and Environmental Microbiology. 81:7644-7655.   10.1128/aem.01895-15   AbstractWebsite

Seasonal variation in the phylogenetic composition of Synechococcus assemblages in estuarine and coastal waters of Hong Kong was examined through pyrosequencing of the rpoC1 gene. Sixteen samples were collected in 2009 from two stations representing estuarine and ocean-influenced coastal waters, respectively. Synechococcus abundance in coastal waters gradually increased from 3.6 x 10(3) cells ml(-1) in March, reaching a peak value of 5.7 x 10(5) cells ml(-1) in July, and then gradually decreased to 9.3 x 10(3) cells ml(-1) in December. The changes in Synechococcus abundance in estuarine waters followed a pattern similar to that in coastal waters, whereas its composition shifted from being dominated by phycoerythrin-rich (PE-type) strains in winter to phycocyanin-only (PC-type) strains in summer owing to the increase in freshwater discharge from the Pearl River and higher water temperature. The high abundance of PC-type Synechococcus was composed of subcluster 5.2 marine Synechococcus, freshwater Synechococcus (F-PC), and Cyanobium. The Synechococcus assemblage in the coastal waters, on the other hand, was dominated by marine PE-type Synechococcus, with subcluster 5.1 clades II and VI as the major lineages from April to September, when the summer monsoon prevailed. Besides these two clades, clade III cooccurred with clade V at relatively high abundance in summer. During winter, the Synechococcus assemblage compositions at the two sites were similar and were dominated by subcluster 5.1 clades II and IX and an undescribed clade (represented by Synechococcus sp. strain miyav). Clade IX Synechococcus was a relatively ubiquitous PE-type Synechococcus found at both sites, and our study demonstrates that some strains of the clade have the ability to deal with large variation of salinity in subtropical estuarine environments. Our study suggests that changes in seawater temperature and salinity caused by the seasonal variation of monsoonal forcing are two major determinants of the community composition and abundance of Synechococcus assemblages in Hong Kong waters.

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
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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.

Stuart, RK, Dupont CL, Johnson AD, Paulsen IT, Palenik B.  2009.  Coastal strains of marine synechococcus species exhibit increased tolerance to copper shock and a distinctive transcriptional response relative to those of open-ocean strains. Applied and Environmental Microbiology. 75:5047-5057.   10.1128/aem.00271-09   AbstractWebsite

Copper appears to be influencing the distribution and abundance of phytoplankton in marine environments, and cyanobacteria are thought to be the most sensitive of the phytoplankton groups to copper toxicity. By using growth assays of phylogenetically divergent clades, we found that coastal strains of marine Synechococcus species were more tolerant to copper shock than open-ocean strains. The global transcriptional response to two levels of copper shock were determined for both a coastal strain and an open-ocean strain of marine Synechococcus species using whole-genome expression microarrays. Both strains showed an osmoregulatory-like response, perhaps as a result of increasing membrane permeability. This could have implications for marine carbon cycling if copper shock leads to dissolved organic carbon leakage in Synechococcus species. The two strains additionally showed a common reduction in levels of photosynthesis-related gene transcripts. Contrastingly, the open-ocean strain showed a general stress response, whereas the coastal strain exhibited a more specifically oxidative or heavy-metal acclimation response that may be conferring tolerance. In addition, the coastal strain activated more regulatory elements and transporters, many of which are not conserved in other marine Synechococcus strains and may have been acquired by horizontal gene transfer. Thus, tolerance to copper shock in some marine Synechococcus strains may in part be a result of a generally increased ability to sense and respond in a more stress-specific manner.

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.

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.

Dyhrman, ST, Palenik B.  2003.  Characterization of ectoenzyme activity and phosphate-regulated proteins in the coccolithophorid Emiliania huxleyi. Journal of Plankton Research. 25:1215-1225.   10.1093/plankt/fbg086   AbstractWebsite

Three phosphate-regulated proteins in the coccolithophorid Emiliania huxleyi were detected by the biotinylation of cell-surface proteins. Two of these phosphate-regulated proteins have reduced denatured molecular weights near I 10 000 Do (118 078 and 110 541, respectively), while the third, and most abundant, is 69 087 Da. Induction of the three proteins and the common marker of phosphate stress, alkaline phosphatase activity, occur in the presence of <0.25 mu M inorganic phosphate in batch culture. Phosphate-regulated proteins and enzyme activity differed among E. huxleyi strains. Alkaline phosphatase is an enzyme commonly induced by phytoplankton in response to phosphate stress in order for cells to scavenge inorganic phosphate from organic sources. In E. huxleyi, this enzyme activity and the phosphate-regulated proteins are rapidly lost when phosphate is added back to phosphate-stressed cultures. This contrasts with the slower loss of alkaline phosphatase activity in the dinoflagellate Prorocentrum minimum. The presence of the three phosphate-regulated proteins and enzyme activity appear to differ somewhat among E. huxleyi strains. Based on these differences between strains, kinetic data, growth experiments and enzyme activities, the 69 087 Da protein may be a phosphatase with a high specificity for 5'-nucleotides.

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.

Davis, AK, Palenik B.  2008.  Characterization of a modular, cell-surface protein and identification of a new gene family in the diatom Thalassiosira pseudonana. Protist. 159:195-207.   10.1016/j.protis.2007.09.006   AbstractWebsite

We report the characterization of a cell-surface protein isolated from copper-stressed cells of the centric diatom Thalassiosira pseudonana Hasle and Heimdal (CCMP 1335). This protein has an apparent molecular weight of 100kDa and is highly acidic. The 100kDa protein (p100) sequence is comprised almost entirely of a novel domain termed TpRCR for T pseudonana repetitive cysteine-rich domain, that is repeated 8 times and that contains conserved aromatic, acidic, and potential metal-binding amino acids. The analysis of the T pseudonana genome suggests that p100 belongs to a large family of modular proteins that consist of a variable number of TpRCR domain repeats. Based on cell surface biotinylation and antibody data, p100 appears to migrate more rapidly with SDS-PAGE when extracted from cells exposed to high levels of copper; however, the discovery of a large family of TpRCR domain-containing proteins leaves open the possibility that the antibody may be crossreacting with members of this protein family that are responding differently to copper. The response of the gene encoding p100 at the mRNA level during synchronized progression through the normal cell cycle is similar to previously characterized genes in T pseudonana encoding cell wall proteins called silaffins. (c) 2007 Elsevier GmbH. All rights reserved.

Johnson, TL, Palenik B, Brahamsha B.  2011.  Characterization of a functional vanadium-dependent bromoperoxidase in the marine cyanobacterium Synechococcus sp. CC9311. Journal of Phycology. 47:792-801.   10.1111/j.1529-8817.2011.01007.x   AbstractWebsite

Vanadium-dependent bromoperoxidases (VBPOs) are characterized by the ability to oxidize halides using hydrogen peroxide. These enzymes are well-studied in eukaryotic macroalgae and are known to produce a variety of brominated secondary metabolites. Though genes have been annotated as VBPO in multiple prokaryotic genomes, they remain un-characterized. The genome of the coastal marine cyanobacterium Synechococcus sp. CC9311 encodes a predicted VBPO (YP_731869.1, sync_2681), and in this study, we show that protein extracts from axenic cultures of Synechococcus possess bromoperoxidase activity, oxidizing bromide and iodide, but not chloride. In-gel activity assays of Synechococcus proteins separated using PAGE reveal a single band having VBPO activity. When sequenced via liquid chromatography/mass spectrometry/mass spectrometry (LC/MS/MS), peptides from the band aligned to the VBPO sequence predicted by the open reading frame (ORF) sync_2681. We show that a VBPO gene is present in a closely related strain, Synechococcus sp. WH8020, but not other clade I Synechococcus strains, consistent with recent horizontal transfer of the gene into Synechococcus. Diverse cyanobacterial-like VBPO genes were detected in a pelagic environment off the California coast using PCR. Investigation of functional VBPOs in unicellular cyanobacteria may lead to discovery of novel halogenated molecules and a better understanding of these organisms' chemical ecology and physiology.