Skip to main content
Article thumbnail
Location of Repository

Characterisation of bacteriophages that infect Acaryochloris

By Yi-Wah Chan


The cyanobacterium Acaryochloris marina was isolated in 1996 and solved a 50 year old mystery as to the origin of the pigment chlorophyll d, which was thought to be a pigment of red algae or a breakdown product of the universal chlorophyll, chlorophyll a. Over the next decade, new Acaryochloris spp. were isolated from all over the world as the genus received international interest from the scientific community, with the majority of research directed towards understanding the mechanisms of photosynthesis of this uniquely pigmented cyanobacterium, using A. marina as the model organism of the genus. During this project, characterisation of different aspects of photosynthesis in Acaryochloris spp. was performed including an investigation of pigment adaptation and composition and the growth and characterisation of A. marina biofilms. However, the main focus of the thesis concerns the isolation and characterisation of cyanophages A-HIS1 and AHIS2, which infect A. marina as a basis to investigate and understand the impact of phage on host physiology in this new model system. A-HIS1 and A-HIS2 were characterised by their morphology, growth behaviour and genomes. Experiments were designed and implemented to investigate interactions between the phages and host. Interestingly, an analysis of novel genes in these phages revealed a surprising evolutionary history of phages A-HIS1 and A-HIS2 providing new insights into the origin of DNA polymerase, which is found only in the mitochondria of eukaryotes

Topics: QR
OAI identifier:

Suggested articles


  1. (1883) Farbe und assimilation.
  2. (1892) ¨ Uber die Kultur und Lebensbedingungen der Meersalgen.
  3. (2005b) The nature of the photosystem II reaction centre in the chlorophyll d-containing prokaryote, Acaryochloris marina. doi
  4. (2007). 410(2-3):428–432, 1997.Bibliography 216 Sophie Martin. Photoelectrochemistry of immobilised photosynthetic components: from chlorophyll to intact chloroplasts.
  5. (2007). 65–73 c
  6. (2007). A computational survey of candidate exonic splicing enhancer motifs in the model plant Arabidopsis thaliana. doi
  7. (1998). A photosystem I reaction center driven by chlorophyll d in oxygenic photosynthesis. doi
  8. (2001). A probabilistic method for identifying start codons in bacterial genomes. doi
  9. (1993). A programmed translational frameshift is required for the synthesis of a bacteriophage lambda tail assembly protein. doi
  10. (2008). A proteomic approach to the identification of the major virion structural proteins of the marine cyanomyovirus S-PM2. Microbiology, 154(Pt 6):1775–1782, doi
  11. (1993). A quantifiable phenotype of viral propagation. doi
  12. (2006). A temporal and spatial investigation of cyanophage abundance in the Gulf of Aqaba, Red Sea. doi
  13. (1998). Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. doi
  14. (2003). Acaryochloris marina gen. et sp. nov. (cyanobacteria), an oxygenic photosynthetic prokaryote containing Chl d as a major pigment. doi
  15. (2009). Active site substitutions delineate distinct classes of eubacterial flap endonuclease. doi
  16. (2007). Advanced sequencing technologies and their wider impact in microbiology. doi
  17. (1994). Amino acid sequence motif of group I intron endonucleases is conserved in open reading frames of group II introns. Trends Biochem Sci, doi
  18. (1976). An analysis of the visible absorption spectrum of chlorophyll a monomer, dimer and oligomers in solution. doi
  19. (1994). An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. doi
  20. (2001). Analysis of six prophages in Lactococcus lactis IL1403: different genetic structure of temperate and virulent phage populations. doi
  21. (2000). Artemis: sequence visualization and annotation. doi
  22. (2001). Bacteriophage latent-period evolution as a response to resource availability. doi
  23. Bacteriophage origins of mitochondrial replication and transcription proteins. doi
  24. (1991). Bacteriophage T4 encodes an RNase H which removes RNA primers made by the T4 DNA replication system in vitro.
  25. (2003). Bacteriophage T4 genome. doi
  26. (2004). Biofilms 2003: emerging themes and challenges in studies of surface-associated microbial life. doi
  27. (1986). Biological and ecological characterisation of the marine unicellular cyanobacterium Synechococcus.
  28. (2006). Biological applications of scanning electrochemical microscopy: chemical imaging of single living cells and beyond. doi
  29. (1980). Biophysical Ecology. doi
  30. (2009). Carrying photosynthesis genes increases ecological fitness of cyanophage in silico. doi
  31. (2007). Chapter 13: Bacteriophages of Listeria. doi
  32. (2006). Chapter 3: Relative quantification.
  33. (1959). Chlorophyll a with the 9-vinyl group replaced by a formyl group.
  34. (1996). Chlorophyll d as a major pigment. doi
  35. (2004). Chlorophyll d in an epiphytic cyanobacterium of red algae. doi
  36. (1943). Chlorophyll d, a green pigment of red algae.
  37. (2005). Chlorophyll d: the puzzle resolved. doi
  38. (2009). Chromatic photoacclimation extends utilisable photosynthetically active radiation in the chlorophyll d-containing cyanobacterium, Acaryochloris marina. Photosynth Res, Epub ahead of print:pp. unknown, doi
  39. (2003). Clade-specific 16S ribosomal DNA oligonucleotides reveal the predominance of a single marine Synechococcus clade throughout a stratified water column in the Red Sea. doi
  40. (2006). Closely related Prochlorococcus genotypes show remarkably different depth distributions in two oceanic regions as revealed by in situ hybridization using 16S rRNA-targeted oligonucleotides.
  41. (1979). Coliphage lambda ghosts obtained by osmotic shock or LiCl treatment are devoid of J- and H-gene products. doi
  42. (2006). Community genomics among stratified microbial assemblages in the ocean’s interior. doi
  43. (2001). Comparative phage genomics and the evolution of Siphoviridae: insights from dairy phages. doi
  44. (2004). Comparative phylogenies of the housekeeping genes atpD, infB and rpoB and the 16S rRNA gene within the Pasteurellaceae. doi
  45. (2007). Comparison of genomes of three Xanthomonas oryzae bacteriophages. doi
  46. (1993). Compilation, alignment, and phylogenetic relationships of DNA polymerases. doi
  47. (1995). Composition of ultraphytoplankton in the central NorthAtlantic. Mar Ecol Prog Ser, doi
  48. (2004). Conserved translational frameshift in dsDNA bacteriophage tail assembly genes. doi
  49. (2006). Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. doi
  50. (2002). CpeR is an activator required for expression of the phycoerythrin operon (cpeBA) in the cyanobacterium Fremyella diplosiphon and is encoded in the phycoerythrin linker-polypeptide operon (cpeCDESTR). doi
  51. (2003). Creating standard curves with genomic DNA or plasmid DNA templates for use in quantitative PCR, 4371090 revision a edition,
  52. (2007). CRISPR provides acquired resistance against viruses in prokaryotes. doi
  53. (2007). Cryopreservation of microalgae and cyanobacteria. doi
  54. (2004). Cyanophage diversity, inferred from g20 gene analyses, in the largest natural lake in France, Lake Bourget. doi
  55. (2007). Cyanophage Pf-WMP4, a T7-like phage infecting the freshwater cyanobacterium Phormidium foveolarum: complete genome sequence and DNA translocation. doi
  56. (2003). Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. doi
  57. (1990). Deletion of rpoB reveals a second distinct transcription system in plastids of higher plants.
  58. (2001). Detection of chlorophyll d0 and pheophytin a in a chlorophyll d-dominating oxygenic photosynthetic prokaryote Acaryochloris marina. doi
  59. (1993). Detection of rifampicin-resistance mutations in Mycobacterium tuberculosis. doi
  60. (2009). Determining the specific microbial populations and their spatial distribution within the stromatolite ecosystem of Shark Bay. doi
  61. (2002). Digital Model 10 and Model 20 Controller.
  62. (2005). Discovery of a free-living chlorophyll d-producing cyanobacterium with a hybrid proteobacterial/cyanobacterial small-subunit rRNA gene. doi
  63. (2005). Discovery of a free-living chlorophyll dproducing cyanobacterium with a hybrid proteobacterial/ cyanobacterial small-subunit rRNA gene. doi
  64. (1977). DNA polymerase of mitochondria is a gamma-polymerase.
  65. (2007). DNA replication and transcription in mammalian mitochondria. Annu Rev Biochem, 76:679– 699, doi
  66. (1996). DNA replication in eukaryotic cells. Chapter 15: Cellular DNA Polymerases. doi
  67. (2005). Ecology: a niche for cyanobacteria containing chlorophyll d. doi
  68. (2005). Effect of iron on growth and ultrastructure of Acaryochloris marina. doi
  69. (2002). Energy equilibration and primary charge separation in chlorophyll dbased photosystem I reaction center isolated from Acaryochloris marina. doi
  70. (2009). Environ Microbiol, Epub ahead of print:pp. unknown,
  71. (1979). Evidence by electron micrographs for a high incidence of bacteriophage particles in the waters of Yaquina Bay, Oregon: ecological and taxonomical implications.
  72. (2008). Evidence of global chlorophyll d. doi
  73. (2002). Evolution of DNA polymerase families: evidences for multiple gene exchange between cellular and viral proteins. doi
  74. (1999). Evolutionary relationships among diverse bacteriophages andBibliography 211 prophages: All the worlds a phage. doi
  75. (2005). Excitation energy transfer from phycobiliprotein to chlorophyll d in intact cells of Acaryochloris marina studied by time- and wavelengthresolved fluorescence spectroscopy. doi
  76. (2001). Exoribonuclease superfamilies: structural analysis and phylogenetic distribution. doi
  77. (2002). Farbe und Assimilation. Bot Z, 41:1–29, 1883.Bibliography 208
  78. (2000). Fluorescence properties of chlorophyll d-dominating prokaryotic alga, Acaryochloris marina: studies using time-resolved fluorescence spectroscopy on intact cells. doi
  79. (2006). Fluorescence properties of the chlorophyll d-dominated cyanobacterium Acarychloris sp. strain Awaji. doi
  80. (2004). From endonucleases to transcription factors: evolution of the AP2 DNA binding domain in plants. doi
  81. (2000). Functional characteristics of chlorophyll d-predominating photosynthetic apparatus in intact cells of Acaryochloris marina.
  82. (1961). Further evidence of the relation between 2-desvinyl-2-formylchlorophyll a and chlorophyll d. doi
  83. (1979). Generic assignments, strain histories and properties of pure cultures of cyanobacteria. doi
  84. (2006). Genome sequence and global gene expression of Q54, a new phage species linking the 936 and c2 phage species of Lactococcus lactis. doi
  85. (2007). Genome sequence, structural proteins, and capsid organization of the cyanophage Syn5: a “horned” bacteriophage of marine Synechococcus. doi
  86. (2007). Genome sequences of two closely related Vibrio parahaemolyticus phages, VP16T and VP16C. doi
  87. (2007). Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. doi
  88. (2008). Genomic analysis of freshwater cyanophage Pf-WMP3 infecting cyanobacterium Phormidium foveolarum: the conserved elements for a phage. doi
  89. (2007). Genomic and structural analysis of Syn9, a cyanophage infecting marine Prochlorococcus and Synechococcus. doi
  90. (2002). Genomic sequence and evolution of marine cyanophage P60: a new insight on lytic and lysogenic phages. doi
  91. (2008). Glucose and lactate biosensors for scanning electrochemical microscopy imaging of single live cells. doi
  92. (1997). Growth and phage resistance of Anabaena sp. strain PCC7120 in the presence of cyanophage AN-15.
  93. H.Bibliography 206 Mann. Transcription of a ’photosynthetic’ T4-type phage during infection of a marine cyanobacterium. doi
  94. (1999). Heuristic approach to deriving models for gene finding. doi
  95. (1989). High abundance of viruses found in aquatic environments. doi
  96. (2004). HNH family subclassification leads to identification of commonality in the His-Me endonuclease superfamily. doi
  97. (2001). Homing endonucleases: structural and functional insight into the catalysts of intron/intein mobility. doi
  98. (1966). Host specificity of DNA produced by Escherichia coli: bacterial mutations affecting the restriction and modification of DNA. doi
  99. (2006). Identification of a diagnostic marker to detect freshwater cyanophages of filamentous cyanobacteria. doi
  100. (2004). Identification of the primary electron donor in PS II of the Chl d-dominated cyanobacterium Acaryochloris marina. doi
  101. (2006). Ig-like domains on bacteriophages: a tale of promiscuity and deceit. doi
  102. (1998). Imaging of cellular activity of single cultured cells by scanning electrochemical microscopy. doi
  103. (2001). in river estuaries. doi
  104. (2002). InBase, the intein database. doi
  105. (2008). Infection by the ‘photosynthetic’ phage S-PM2 induces increased synthesis of phycoerythrin doi
  106. (1999). Int Rev Cytol,
  107. (2000). Invasion of a multitude of genetic niches by mobile endonuclease genes. doi
  108. (1993). Isolation and molecular characterization of five marine cyanophages propagated on Synechococcus sp. strain WH7803.
  109. (1988). Isolation and purification of cyanobacteria. doi
  110. (2009). Isolation of cyanophages from aquatic environments. doi
  111. (1993). Kinetic PCR analysis: real-time monitoring of DNA amplification reactions. doi
  112. L’action bactericide des eaux de la Jumna et du Gange sur le vibrion du cholera.
  113. Larkum A & Barber J (2005a) Iron deficiency induces a chlorophyll d-binding Pcb antenna system around Photosystem Iin Acaryochloris marina. doi
  114. (1997). Light-harvesting in Acaryochloris marina – spectroscopic characterization of a chlorophyll d-dominated photosynthetic antenna system. doi
  115. (1997). Lightharvesting in Acaryochloris marina - spectroscopic characterization of a chlorophyll d-dominated photosynthetic antenna system. doi
  116. (1996). Lysogenic conversion by a filamentous phage encoding cholera toxin. doi
  117. (2006). Marine cyanophages and light. doi
  118. (1993). Marine cyanophages infecting oceanic and coastal strains of Synechococcus: abundance, morphology, crossinfectivity and growth characteristics. Mar Ecol Prog Ser, doi
  119. (2007). Marine viruses – major players in the global ecosystem. doi
  120. (1998). Microbial gene identification using interpolated Markov models. doi
  121. (2005). Minor but key chlorophylls in photosystem II. doi
  122. (1999). Mitochondrial evolution. doi
  123. (2008). Modeling the fitness consequences of a cyanophage-encoded photosynthesis gene. doi
  124. (2006). Modular structure of the receptor binding proteins of Lactococcus lactis phages: the RBP structure of the temperate phage TP901-1. doi
  125. (2002). Molecular Biology of the Cell, Fourth Edition. doi
  126. (1996). Molecular cloning of Drosophila mus308, a gene involved in DNA cross-link repair with homology to prokaryotic DNA polymerase I genes.
  127. (1982). Molecular Cloning: doi
  128. (2006). Molecular detection of epiphytic Acaryochloris spp. on marine macroalgae. doi
  129. (1999). Molecular structure, localization and function of biliproteins in the chlorophyll a/d containing oxygenic photosynthetic prokaryote Acaryochloris marina. doi
  130. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. doi
  131. (2001). MRBAYES: Bayesian inference of phylogenetic trees. doi
  132. (2002). Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics, doi
  133. (1943). Mutations of bacteria from virus sensitivity to virus resistance.
  134. (2008). Niche adaptation and genome expansion in the chlorophyll d-producing cyanobacterium Acaryochloris marina. doi
  135. (1996). Non-orthologous gene displacement. doi
  136. (1985). Novel role for phycoerythrin in a marine cyanobacterium, Synechococcus strain DC2. doi
  137. (1997). Numerical dominance of a group of marine bacteria in the alpha-subclass of the class Proteobacteria in coastal seawater.
  138. (1977). Occurrence and nature of chromatic adaptation in Cyanobacteria. doi
  139. (1998). Occurrence of a sequence in marine cyanophages similar to that of T4 g20 and its application to PCR-based detection and quantification techniques.
  140. (2003). Phage as agents of lateral gene transfer. doi
  141. (2004). Phage taxonomy: we agree to disagree. doi
  142. (2004). PHIRE, a deterministic approach to reveal regulatory elements in bacteriophage genomes. doi
  143. (2005). Photosynthesis genes in marine viruses yield proteins during host infection. doi
  144. (1997). Photosynthetic electron transport in single guard cells as measured by scanning electrochemical microscopy.
  145. (1982). Phycobilisomes: structure and dynamics. doi
  146. (2009). Phylogenetic analysis indicates evolutionary diversity and environmental segregation of marine podovirus DNA polymerase gene sequences. doi
  147. (2002). Phylogenetic diversity of marine cyanophage isolates and natural virus communities as revealed by sequences of viral capsid assembly protein gene g20. doi
  148. (1998). Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes.
  149. (2003). Phytoplankton analyzer. PHYTO-PAM and Phyto-Win Software V 1.45. System components and principles of operation.
  150. (2007). Pigment composition and adaptation in free-living and symbiotic strains of Acaryochloris marina. doi
  151. (1997). Pigment composition of a novel oxygenic photosynthetic prokaryote containing chlorophyll d as the major chlorophyll. doi
  152. (2000). Prediction of transcription terminators in bacterial genomes. doi
  153. (2008). Prevalence of highly host-specific cyanophages in the estuarine environment. doi
  154. (2007). Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol, 132:365–386, 2000.Bibliography 221 doi
  155. (1997). Prochlorococcus growth rate and contribution to primary production in the equatorial and subtropical North Pacific Ocean. Aquat Microb Ecol, doi
  156. (1999). Prochlorococcus, a marine photosynthetic prokaryote of global significance. doi
  157. (2002). Protein identification by in-gel digestion and mass spectrometric analysis. doi
  158. (1985). Purification and characterization of Escherichia coli RNase T. doi
  159. (2009). Quantification of host and phage mRNA expression during infection using real-time PCR. doi
  160. (1999). Quantification of murine cytokine mRNAs using real time quantitative reverse transcriptase PCR. doi
  161. (2007). Rapid, accurate, computational discovery of Rho-independent transcription terminators illuminates their relationship to DNA uptake. doi
  162. (1984). Ribonuclease T: new exoribonuclease possibly involved in end-turnover of tRNA. doi
  163. (2005). RNA-dependent DNA polymerase (rt) activity of bacterial DNA polymerases.
  164. (1985). RNase T is responsible for the end-turnover of tRNA in Escherichia coli. doi
  165. (1995). Seasonal abundance of Prochlorococcus in Suruga Bay, Japan in 1992-1993. doi
  166. (1997). Seasonal and spatial variability in phytoplankton biomass, productivity andBibliography 225 growth in the north-western Indian Ocean: the southwest and northeast monsoon, 1992-1993. Deep Sea Res Part I-Oceanographic doi
  167. Sequence analysis of an archaeal virus isolated from a hypersaline lake in Inner Mongolia, doi
  168. (2008). Small CRISPR RNAs guide antiviral defense in prokaryotes. doi
  169. (1964). Smoothing and differentiation of data by simplified least square procedures. doi
  170. (1964). Smoothing and differentiation of data by simplified least square procedures. Anal Chem, doi
  171. sp. an oxyphototrophic marine prokaryote containing divinyl chlorophyll a and b. doi
  172. (1973). Structural proteins of bacteriophage T5. doi
  173. (1992). subsp. pastoris subsp. nov. strain PCC 9511, the first axenic chlorophyll a2/b2-containing cyanobacterium (Oxyphotobacteria).
  174. (1973). Synthesis and functions of the -C-C-A terminus of transfer RNA. doi
  175. (1998). Taxonomy of bacterial viruses: establishment of tailed virus genera and the order Caudovirales. Arch Virol, doi
  176. (2006). Tech Note:
  177. (2006). Temporal order of evolution of DNA replication systems inferred by comparison of cellular and viral DNA polymerases.
  178. (1994). The characterisation of a mammalian DNA structure-specific endonuclease.
  179. (1996). The effect of phosphate status on the kinetics of cyanophage infection in the oceanic cyanobacterium Synechococcus sp. doi
  180. (2005). The genome of S-PM2, a “photosynthetic” T4-type bacteriophage that infects marine Synechococcus strains. doi
  181. (2002). The major light-harvesting pigment protein of Acaryochloris marina. doi
  182. (1993). The marine prochlorophyte Prochlorococcus contributes significantly to phytoplankton biomass and primary production in the Sargasso Sea. Deep-Sea Res Part I-Oceanographic Res Pap, doi
  183. (2006). The minor capsid protein gp7 of bacteriophage SPP1 is required for efficient infection of Bacillus subtilis. doi
  184. (1970). The morphogenesis of bacteriophage lambda. II. Identification of the principal structural proteins. doi
  185. (2009). The nature of the photosystem II reaction centre in the chlorophyll d-containing prokaryote, Acaryochloris marina. doi
  186. (1964). The operon: on its third anniversary. doi
  187. (2002). The phylogenetic distribution of bacterial ribonucleases. doi
  188. (2008). The primary electron donor of photosystem II of the cyanobacterium Acaryochloris marina is a chlorophyll d and the water oxidation is driven by a chlorophyll a/chlorophyll d heterodimer. doi
  189. (2004). The Quantitative PCR Technical Guide. 3050 Spruce St., St. Louis, MO 63103, 2008.Bibliography 223
  190. (1989). The rise of atmospheric oxygen. doi
  191. (2007). The Sorcerer II Global Ocean Sampling expedition: expanding the universe of protein families. doi
  192. (2000). The terminase enzyme from bacteriophage lambda: a DNApackaging machine. doi
  193. (2005). The third age of phage. doi
  194. (1995). The tRNA processing enzyme RNase T is essential for maturation of 5S RNA. doi
  195. (2001). Transfer of the Salmonella type III effector sopE between unrelated phage families. doi
  196. (2001). TreeView: an application to display phylogenetic trees on personal computers. doi
  197. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. doi
  198. Twinkle, the mitochondrial replicative DNA helicase, is widespread in the eukaryotic radiation and may also be the mitochondrial DNA primase in most eukaryotes. doi
  199. (2007). Ultrastructural and genetic characteristics of endolithic cyanobacterial biofilms colonizing Antarctic granite rocks. doi
  200. (2000). Uphill energy transfer in a chlorophyll d-dominating oxygenic photosynthetic prokaryote, doi
  201. (2002). ussow. The dilemma of phage taxonomy illustratedBibliography 220 by comparative genomics of Sfi21-like Siphoviridae in lactic acid bacteria. doi
  202. (1996). Vertical distributions and photosynthetic action spectra of two oceanic picophytoplankters, doi
  203. (2005). Viral genome packaging machines: genetics, structure, and mechanism. doi
  204. (2005). Viral proteins functioning in organelles: a cryptic origin? doi
  205. Virus isolation studies suggest short-term variations in abundance in natural cyanophage populations of the Indian Ocean. doi
  206. (2008). Virus population dynamics and acquired virus resistance in natural microbial communities. doi
  207. (2005). Viruses in the sea. doi
  208. (1986). Visualization of bilin-linked peptides and proteins in polyacrylamide gels. doi
  209. (2004). W.Bibliography 214 Chisholm. Transfer of photosynthesis genes to and from Prochlorococcus viruses. doi

To submit an update or takedown request for this paper, please submit an Update/Correction/Removal Request.