Diversity of the ribulose bisphosphate carboxylase/oxygenase form I gene (rbcL) in natural phytoplankton communities

The phytoplankton of the world's oceans play an integral part in global carbon cycling and food webs by conversion of carbon dioxide into organic carbon. They accomplish this task through the action of the Calvin cycle enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO). Here we have investigated the phylogenetic diversity in the form I rbcL locus in natural phytoplankton communities of the open ocean and representative clones of marine autotrophic picoplankton by mRNA or DNA amplification and sequencing of a 480 to 483 bp internal fragment of this gene. Five gene sequences were recovered from nucleic acids of natural phytoplankton communities of the Gulf of Mexico. The rbcL genes of two Prochlorococcus isolates and one Synechococcus strain (WH8007) were also sequenced. Sequences were aligned with the database of rbcL genes and subjected to both neighbor-joining and parsimony analyses. The five sequences from the natural phytoplankton community spanned nearly the entire diversity of characterized form I rbcL genes, with some sequences closely related to isolates such as Synechococcus and Prochlorococcus (forms IA and I) and prymnesiophyte algae (form ID), while other sequences were deeply rooted. Unexpectedly, the deep euphotic zone contained an organism that possesses a transcriptionally active rbcL gene closely related to that of a recently characterized manganese-oxidizing bacterium, suggesting that such chemoautotrophs may contribute to the diversity of carbon-fixing organisms in the marine euphotic zone.

[1]  J. Paul,et al.  Analysis of Ribulose Bisphosphate Carboxylase Gene Expression in Natural Phytoplankton Communities by Group-Specific Gene Probing , 1997 .

[2]  F. Tabita,et al.  Microbial ribulose 1,5-bisphosphate carboxylase/oxygenase: a molecule for phylogenetic and enzymological investigation. , 1997, FEMS microbiology letters.

[3]  R. Caspi,et al.  Unusual ribulose-1,5-bisphosphate carboxylase/oxygenase genes from a marine manganese-oxidizing bacterium. , 1996, Microbiology.

[4]  J. Paul,et al.  Regulation of Ribulose Bisphosphate Carboxylase Gene Expression in Natural Phytoplankton Communities .1. Diel Rhythms , 1996 .

[5]  B. Palenik,et al.  CYANOBACTERIAL EVOLUTION AND PROCHLOROPHYTE DIVERSITY AS SEEN IN DNA‐DEPENDENT RNA POLYMERASE GENE SEQUENCES 1 , 1996 .

[6]  Roderic D. M. Page,et al.  TreeView: an application to display phylogenetic trees on personal computers , 1996, Comput. Appl. Biosci..

[7]  J. Palmer,et al.  Rampant horizontal transfer and duplication of rubisco genes in eubacteria and plastids. , 1996, Molecular biology and evolution.

[8]  F. Tabita,et al.  Ribulose-1,5-bisphosphate carboxylase/oxygenase gene expression and diversity of Lake Erie planktonic microorganisms , 1996, Applied and environmental microbiology.

[9]  S. Miyachi,et al.  Vertical distributions and photosynthetic action spectre of two oceanic picophytopianlcters,Prochlorococcus marinus andSynechococcus sp. , 1996 .

[10]  D. Yellowlees,et al.  Rubisco in marine symbiotic dinoflagellates: form II enzymes in eukaryotic oxygenic phototrophs encoded by a nuclear multigene family. , 1996, The Plant cell.

[11]  J. Paul,et al.  Molecular Approaches to Studying Natural Communities of Autotrophs , 1996 .

[12]  H. Yamazaki.  Regulation of ribulose bisphosphate carboxylase gene expression in natural phytoplankton communities. I. Diel rhythms , 1996 .

[13]  G. Preston.  Polymerase chain reaction with degenerate oligonucleotide primers to clone gene family members. , 1996, Methods in molecular biology.

[14]  J. Palmer,et al.  Rubisco rules fall; gene transfer triumphs. , 1995, BioEssays : news and reviews in molecular, cellular and developmental biology.

[15]  Y. van de Peer,et al.  An early origin of plastids within the cyanobacterial divergence is suggested by evolutionary trees based on complete 16S rRNA sequences. , 1995, Molecular biology and evolution.

[16]  R. Mitchell,et al.  Engineering Rubisco to change its catalytic properties , 1995 .

[17]  D. Bhattacharya,et al.  THE PHYLOGENY OF PLASTIDS: A REVIEW BASED ON COMPARISONS OF SMALL‐SUBUNIT RIBOSOMAL RNA CODING REGIONS , 1995 .

[18]  D. Morse,et al.  A nuclear-encoded form II RuBisCO in dinoflagellates. , 1995, Science.

[19]  A. Yokota,et al.  Distribution of fallover in the carboxylase reaction among ribulose 1,5-bisphosphate carboxylase/oxygenases of photosynthetic organisms , 1995 .

[20]  J. Palmer,et al.  Phylogenetic analysis of tufA sequences indicates a cyanobacterial origin of all plastids. , 1995, Molecular phylogenetics and evolution.

[21]  R. Andersen,et al.  Cladistic analyses of combined traditional and molecular data sets reveal an algal lineage. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[22]  J. Fuhrman,et al.  Phylogenetic diversity of subsurface marine microbial communities from the Atlantic and Pacific Oceans , 1993, Applied and environmental microbiology.

[23]  N. Chernykh.  Detection of the ribulose bisphosphate carboxylase gene in natural samples by polymerase chain reaction , 1995 .

[24]  V. Savolainen,et al.  Chloroplast DNA sequences from a miocene diatomite deposit in Ardèche (France) , 1995 .

[25]  J. Paul,et al.  Extraction of DNA and RNA from Aquatic Environments , 1995 .

[26]  F. Tabita.  The Biochemistry and Metabolic Regulation of Carbon Metabolism and CO2 Fixation in Purple Bacteria , 1995 .

[27]  M. Madigan,et al.  Anoxygenic Photosynthetic Bacteria , 1995, Advances in Photosynthesis and Respiration.

[28]  B. Palenik.  Cyanobacterial community structure as seen from RNA polymerase gene sequence analysis , 1994, Applied and environmental microbiology.

[29]  B. Read,et al.  High substrate specificity factor ribulose bisphosphate carboxylase/oxygenase from eukaryotic marine algae and properties of recombinant cyanobacterial RubiSCO containing "algal" residue modifications. , 1994, Archives of biochemistry and biophysics.

[30]  D. Karl,et al.  Estimation of diversity and community structure through restriction fragment length polymorphism distribution analysis of bacterial 16S rRNA genes from a microbial mat at an active, hydrothermal vent system, Loihi Seamount, Hawaii , 1994, Applied and environmental microbiology.

[31]  L. Shapiro,et al.  Immunochemical characterization for eukaryotic ultraplankton from the Atlantic and Pacific oceans , 1994 .

[32]  M. A. Steel,et al.  Confidence in evolutionary trees from biological sequence data , 1993, Nature.

[33]  M T Clegg,et al.  Chloroplast gene sequences and the study of plant evolution. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[34]  M. Becker‐André,et al.  Absolute levels of mRNA by polymerase chain reaction-aided transcript titration assay. , 1993, Methods in enzymology.

[35]  J. Paul,et al.  Ribulose-Bisphosphate Carboxylase Gene Expression in Subtropical Marine Phytoplankton Populations , 1993 .

[36]  J. Murrell,et al.  Microbial growth on C[1] compounds , 1993 .

[37]  V. Jung,et al.  Cloning of polymerase chain reaction-generated DNA containing terminal restriction endonuclease recognition sites. , 1993, Methods in enzymology.

[38]  E. Delong.  Archaea in coastal marine environments. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[39]  S. Chisholm,et al.  Multiple evolutionary origins of prochlorophytes within the cyanobacterial radiation , 1992, Nature.

[40]  R. Haselkorn,et al.  Multiple evolutionary origins of prochlorophytes, the chlorophyllb-containing prokaryotes , 1992, Nature.

[41]  J. Paul,et al.  Detection of Gene Expression in Genetically Engineered Microorganisms and Natural Phytoplankton Populations in the Marine Environment by mRNA Analysis , 1991, Applied and environmental microbiology.

[42]  D. Townsend,et al.  DNA POLYMORPHISM WITHIN THE WH7803 SEROGROUP OF MARINE SYNECHOCOCCUS SPP. (CYANOBACTERIA) 1, 2 , 1990 .

[43]  J. Paul,et al.  Amplification of the rbcL gene from dissolved and particulate DNA from aquatic environments , 1990, Applied and environmental microbiology.

[44]  S. Giovannoni,et al.  Genetic diversity in Sargasso Sea bacterioplankton , 1990, Nature.

[45]  M. Clegg,et al.  Chloroplast DNA sequence from a Miocene Magnolia species , 1990, Nature.

[46]  J. Zehr,et al.  Use of degenerate oligonucleotides for amplification of the nifH gene from the marine cyanobacterium Trichodesmium thiebautii , 1989, Applied and environmental microbiology.

[47]  J. Waterbury,et al.  [6] Isolation and growth of marine planktonic cyanobacteria , 1988 .

[48]  Wen-Hsiung Li,et al.  Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. , 1987, Proceedings of the National Academy of Sciences of the United States of America.