Acta Scientific Microbiology (ISSN: 2581-3226)

Research Article Volume 6 Issue 10

The Lack of Concordance in Evolutionary Pattern of Carboxysome Proteins – Repercussions of HGT or Diverse Evolutionary Potential?

Gurpreet Kaur Sidhu1, Panchsheela Nogia1, Vandana Tomar1, Rajesh Mehrotra2 and Sandhya Mehrotra2

1Plant Molecular Biology and Biochemistry Laboratory, Birla Institute of Technology and Science, Department of Biological Sciences, Pilani, India
2Department of Biological Sciences, Birla Institute of Technology and Science, KK Birla Goa Campus, Zuarinagar, Goa, India

*Corresponding Author: Sandhya Mehrotra, Department of Biological Sciences, Birla Institute of Technology and Science, KK Birla Goa Campus, Zuarinagar, Goa, India.

Received: August 10, 2023; Published: September 23, 2023


Carboxysomes are microcompartments enclosing the primary photosynthetic enzyme Ribulose 1, 5 Bisphosphate Carboxylase/Oxygenase (RuBisCO), an adaptation to help overcome the loose specificity of the latter for carbon dioxide. These carboxysomes, which exist in cyanobacteria and a few other eubacteria are composed of a protein shell wherein a well organized multi-protein assembly acts as the carbon concentrating mechanism (CCM). The present study was conducted to find out the presence/absence of the carboxysome forming proteins across various phyla of eubacteria in order to trace their evolutionary path. The analysis was conducted using the CCM proteins of Gloeobacter violaceus PCC 7421, an early diverging cyanobacterium.
While α carboxysome proteins are also found in other phyla of eubacteria such as proteobacteria, complete set of β carboxysome constituting proteins are found only in β cyanobacteria. The study supports the fact that shell proteins of carboxysomes are evolutionarily linked to shell proteins of microcompartments involved in ethanolamine utilization and propanediol utilization pathways. Moreover, the CcmM and CcmN proteins have possibly originated by domain shuffling or gene fusion like mechanisms. The CcmM, CcmN and CcmO, the multidomain proteins were found to have an evolutionary pattern different from that of CcmK and CcmL leading to cumulative effect on phylogeny of complete operon which was found to be only moderately similar to most conserved regions of genome. The latter (CcmK and CcmL) also being more conserved suggest less robustness to mistranslation possibly due to tight selection of the protein structure evidently responsible for creating an environment suitable for microcompartment pathway it encloses.

 Keywords: Carbon Concentrating Mechanism; Carboxysome; BMC Domain; Domain Shuffling; Microcompartment; Evolution


  1. Jensen T and Bowen C. “Organization of the centroplasm in Nostoc punctiforme”. Proceedings of the Iowa Academy of Science 68 (1961): 89-96.
  2. Kerfeld CA., et al. “Bacterial microcompartments”. Annual Review of Microbiology 64 (2010): 391-408.
  3. Penrod J T and Roth JR. “Conserving a volatile metabolite: a role for carboxysome - like organelles in Salmonella enteric”. Journal of Bacteriology 188 (2006): 2865-2874.
  4. Sampson EM and Bobik T A. “Microcompartments for B-12 dependent 1,2-propanediol degradation provide protection from DNA and cellular damage by a reactive metabolic intermediate. Journal of Bacteriology 190 (2008): 2966-2971.
  5. Huseby D L and Roth JR. “Evidence that a metabolic microcompartment contains and recycles private cofactor pools”. Journal of Bacteriology 195 (2013): 2864-2879.
  6. Chen P., et al. “The control region of the pdu/cob regulon in Salmonella typhimurium”. Journal of Bacteriology 176 (1994): 5474-5482.
  7. Kofoid E., et al. “The 17-gene ethanolamine (eut) operon of Salmonella typhimurium encodes five homologues of carboxysome shell proteins. Journal of Bacteriology 181 (1999): 5317-5329.
  8. Badger MR., et al. “The diversity and coevolution of rubisco, plastids, pyrenoids and chloroplast based CO2 concentrating mechanisms in algae”. Canadian Journal of Botany 76 (1998): 1052-1071.
  9. Kaplan A and Reinhold L. “CO2-concentrating mechanisms in photosynthetic microorganisms”. Annual Review of Plant Physiology and Plant Molecular Biology 50 (1999): 539-570.
  10. Badger M R., et al. “Evolution and diversity of CO2 concentrating mechanisms in cyanobacteria”. Functional Plant Biology 29 (2002): 161-173.
  11. Cannon GC., et al. “Carboxysome genomics: a status report”. Functional Plant Biology 29 (2002): 175-182.
  12. Tanaka S., et al. “Atomic level models of the bacterial carboxysome shell”. Science 319 (2008): 1083-1086.
  13. Price G D., et al. “Advances in understanding the cyanobacterial CO2-concentrating mechanism (CCM): Functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants”. Journal of Experimental Botany (2007).
  14. Alber BE and Ferry JG. “A carbonic anhydrase from the archaeon Methanosarcina thermophila”. Proceedings of the National Academy of Sciences of the United States of America 91 (2013): 6909-6913.
  15. Pena KL., et al. “Structural basis of the oxidative activation of the carboxysomal gamma carbonic anhydrases, CcmM”. Proceedings of the National Academy of Sciences of the United States of America 107 (2010): 2455-2460.
  16. Espie GS and Kimber M S. “Carboxysomes: cyanobacterial Rubisco comes in small packages”. Research 109 (2011): 7-20.
  17. Price GD., et al. “Analysis of a genomic DNA region from the cyanobacterium Synechococcus sp str PCC 7942. Journal of Bacteriology 175 (1993): 2871-2879.
  18. Long B M., et al. “Analysis of carboxysomes from Synechococcus PCC 7942 reveals multiple RuBisCO complexes with carboxysomal proteins CcmM and CcaA”. Journal of Biological Chemistry 282 (2007): 29323-29335.
  19. Kinney J N., et al. “Elucidating essential role of conserved carboxysomal protein CcmN reveals common feature of bacterial microcompartment assembly”. Journal of Biological Chemistry 287 (2012): 17729-17736.
  20. Havemann GD and Bobik T A. “Protein content of polyhedral organelles involved in coenzyme B12-dependent degradation of 1,2-propanediol in Salmonella enetrics serovar typhimurium LT2. Journal of Bacteriology 185 (2003): 5086-5095.
  21. Rae BD., et al. “Functions, Compositions and Evolution of the two types of carboxysomes: Polyhedral Microcompartments that facilitate CO2 fixation in Cyanobacteria and some Proteobacteria”. Microbiology and Molecular Biology Reviews 77 (2013): 357-379.
  22. Menon B B., et al. “Halothiobacillus neopolitanus carboxysomes sequester heterologous and chimeric rubisco species”. pLOS One 3 (2008): e3570.
  23. Fan C G., et al. “Interactions between the termini of lumen enzymes and shell proteins mediate enzyme encapsulation into bacterial microcompartments”. Proceedings of the National Academy of Sciences of the United States of America 109 (2012): 14995-15000.
  24. McClelland M., et al. “Complete genome sequence of Salmonella enteric serovar typhimurium LT2”. Nature 413 (2001): 852-856.
  25. Price G D., et al. “The cyanobacterial CCM as a source of genes for improving photosynthetic CO2 fixation in crop species”. Journal of Experimental Botany 64 (2013): 753-768.
  26. Corchero J L and Cedano J. “Self-assembling, protein-based intracellular bacterial organelles: emerging vehicles for encapsulating, targeting and delivering therapeutical cargoes”. Microbial Cell Factories 10 (2011): 92.
  27. Gaurav V., et al. “Sequence Matrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information”. Cladistics 27 (2010): 171-180.
  28. Thompson JD., et al. “CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice”. Nucleic Acids Research 22 (1994): 4673-4680.
  29. Sela I., et al. “GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters”. Nucleic Acids Research (2015): W7-W14.
  30. Landan G and Graur D. “Local reliability measures from sets of co-optimal multiple sequence alignments”. Pacific Symposium on Biocomputing 13 (2008): 15-24.
  31. Tamura K., et al. “MEGA6: Molecular Evolutionary Genetics Analysis version 6.0”. Molecular Biology and Evolution 30 (2013): 2725-2729.
  32. Nei M and Kumar S. “Molecular Evolution and Phylogenetics”. Oxford University Press, New York (2000).
  33. Altschul S F., et al. “Basic local alignment search tool”. Journal of Molecular Biology 215 (2000): 403-410.
  34. Altschul S F., et al. “Gapped BLAST and PSI-BLAST: a new generation of protein database search programs”. Nucleic Acids Research 25 (1997): 3389-3402.
  35. Geer LY., et al. “CDART: Protein Homology by Domain Architecture”. Genome Research 12 (2002): 1619-1623.
  36. Tajima F and Nei M. “Estimation of evolutionary distance between nucleotide sequences”. Molecular Biology and Evolution 1 (1984): 269-285.
  37. Jukes T H and Cantor C R. “Evolution of protein molecules”. In Munro HN, editor, Mammalian Protein Metabolism, Academic Press, New York (1969).
  38. Nelissen B., et al. “An early origin of plastids within the cyanobacterial divergence is suggested by evolutionary trees based on complete 16S rRNA sequences”. Molecular Biology and Evolution12 (1995): 1166-1173.
  39. Memon D., et al. “A global analysis of adaptive evolution of operons in cyanobacteria”. Van. Leeuwenhoek. 103 (2013): 331-346.
  40. Gupta R S and Mathews D W. “Signature proteins for the major clades of Cyanobacteria”. BMC Evolution and Biology 10 (2010): 24.
  41. Dvořák P., et al. “Morphological and molecular studies of Neosynechococcus sphagnicola, gen. et sp. nov. (Cyanobacteria, Synechococcales)”. Phytotaxa1 (2014): 024-034.
  42. Soo RM., et al. “An expanded genomic representation of the phylum cyanobacteria”. Genome Biology and Evolution 6 (2014): 1031-1045.
  43. Di Rienzi SC., et al. “The human gut and groundwater harbor non-photosynthetic bacteria belonging to a new candidate phylum sibling to Cyanobacteria”. Elife 2 (2013): e01102.
  44. Rippka R., et al. “A cyanobacterium which lacks thylakoids”. Archives of Microbiology 100 (1974): 419-436.
  45. Guglielmi G., et al. “The structure of Gloeobacter violaceus and its phycobilisomes”. Archives of Microbiology 129 (1981): 181-189.
  46. Salstam E and Campbell D. “Membrane lipid composition of the unusual cyanobacterium Gloeobacter violaceus PCC 7421, which lacks sulfoquinovosyl diacylglycerol”. Archives of Microbiology 166 (1996): 132-135.
  47. Frank S., et al. “Bacterial microcompartments moving into a synthetic biological world”. Journal of Biotechnology 163 (2013): 273-279.
  48. Vogel C., et al. “Structure, function and evolution of multidomain proteins”. Current Opinion in Structural Biology 14 (2004): 208-216.
  49. Enright A J., et al. “Protein interaction maps for complete genomes based on gene fusion events”. Nature 402 (1999): 86-90.
  50. Marcotte E M., et al. “A combined algorithm for genome-wide prediction of protein function”. Nature 402 (1999): 83-86.
  51. Snel B., et al. “Genome evolution: Gene fusion versus gene fission”. Trends in Genetics 16 (2000): 9-11.
  52. Yanai I., et al. “Evolution of gene fusions: horizontal transfer versus independent events”. Genome Biology 3 (2002): research0024.
  53. Abdul-Rahman F., et al. “The distribution of polyhedral bacterial microcompartments suggests frequent horizontal transfer and operon reassembly”. Journal of Phylogenetics and Evolutionary Biology 1 (2013): 1-7.
  54. Price MN., et al. “The life-cycle of operons”. PLoS Genetics 2 (2006): e96.
  55. Kumar S. “Molecular clocks: four decades of evolution”. Nature Reviews Genetics 6 (2005): 654-662.
  56. Csaba Pál., et al. “An integrated view of protein evolution”. Nature Reviews Genetics 7 (2006): 337-348.


Citation: Sandhya Mehrotra., et al. “The Lack of Concordance in Evolutionary Pattern of Carboxysome Proteins – Repercussions of HGT or Diverse Evolutionary Potential?".Acta Scientific Microbiology 6.10 (2023): 41-60.


Copyright: © 2023 Sandhya Mehrotra., et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


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