Branching and intercellular communication in the Section V cyanobacterium Mastigocladus laminosus, a complex multicellular prokaryote

Molecular Microbiology

Volumn 91, Issue 5, 2014, Pages 935-949

  Nürnberg, Dennis J ^a   Mariscal, Vicente ^b   Parker, Jamie ^a   Mastroianni, Giulia ^a   Flores, Enrique ^b   Mullineaux, Conrad W ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF SEVILLE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

6 CARBOXYFLUORESCEIN; BACTERIAL PROTEIN; PROTEIN SEPJ; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BIOLOGICAL MONITORING; BRANCHING MORPHOGENESIS; CELL COMMUNICATION; CELL FATE; CELL GROWTH; CELL JUNCTION; CELL MOTION; CELL STRUCTURE; CELL VOLUME; CONTROLLED STUDY; CYANOBACTERIUM; CYTOPLASM; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENE IDENTIFICATION; MASTIGOCLADUS LAMINOSUS; MEMBRANE STRUCTURE; MOLECULAR BIOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROKARYOTE; RANDOMIZATION; SEPJ GENE; SIGNAL TRANSDUCTION; TRICHOME;

MASTIGOCLADUS LAMINOSUS; PROKARYOTA;

CYANOBACTERIA; FLUORESCEINS; FLUORESCENT ANTIBODY TECHNIQUE; MOLECULAR SEQUENCE DATA; PROKARYOTIC CELLS;

EID: 84896717699     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12506     Document Type: Article

References (66)

1. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
2. Anagnostidis, K., and Komárek, J. (1990) Modern approach to the classification system of Cyanophytes. 5-Stigonematales. Arch Hydrobiol Suppl Algol Stud 59: 1-73.
3. Balkwill, D.L., Nierzwicki-Bauer, S.A., and Stevens, S.E.J. (1984) Modes of cell division and branch formation in the morphogenesis of the cyanobacterium Mastigocladus laminosus. J Gen Microbiol 130: 2079-2088.
4. Bekker, A., Holland, H.D., Wang, P.-L., Rumble, D., Stein, H.J., Hannah, J.L., etal. (2004) Dating the rise of atmospheric oxygen. Nature 427: 117-120.
5. Benson, D.A., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J., and Sayers, E.W. (2011) GenBank. Nucleic Acids Res 39: D32-D37.
6. Brown, I.I., Bryant, D.A., Casamatta, D., Thomas-Keprta, K.L., Sarkisova, S.A., Shen, G., etal. (2010) Polyphasic characterization of a thermotolerant siderophilic filamentous cyanobacterium that produces intracellular iron deposits. Appl Environ Microbiol 76: 6664-6672.
7. Buikema, W.J., and Haselkorn, R. (1991) Characterization of a gene controlling heterocyst differentiation in the cyanobacterium Anabaena 7120. Genes Dev 5: 321-330.
8. Butler, R.D., and Allsopp, A. (1972) Ultrastructural investigations in the Stigonemataceae (Cyanophyta). Arch Microbiol 82: 283-299.
9. Campbell, E.L., and Meeks, J.C. (1989) Characteristics of hormogonia formation by symbiotic Nostoc spp. in response to the presence of Anthoceros punctatus or its extracellular products. Appl Environ Microbiol 55: 125-131.
10. Castenholz, R.W. (1976) The effect of sulfide on the bluegreen algae of hot springs. New Zealand and Iceland. J Phycol 12: 54-68.
11. Castenholz, R.W. (1988) Culturing methods for cyanobacteria. Methods Enzymol 167: 68-93.
12. Cohn, F. (1862) Über die Algen des Karlsbader Sprudels, mit Rücksicht auf die Bildung des Sprudelsinsters. Abhandlungen der schlesischen Gesellschaft für vaterländische Kultur 5: 37-55.
13. Croft, W.N., and George, E.A. (1959) Blue-green algae from the Middle Devonian of Rhynie, Aberdeenshire. Bull Br Mus Nat Hist Geol 3: 341-353.
14. Dagan, T., Roettger, M., Stucken, K., Landan, G., Koch, R., Major, P., etal. (2013) Genomes of stigonematalean cyanobacteria (Subsection V) and the evolution of oxygenic photosynthesis from prokaryotes to plastids. Genome Biol Evol 5: 31-44.
15. Desikachary, T.V. (1959) Cyanophyta. New Delhi, India: Indian Council of Agricultural Research.
16. Finsinger, K., Scholz, I., Serrano, A., Morales, S., Uribe-lorio, L., Mora, M., etal. (2008) Characterization of true-branching cyanobacteria from geothermal sites and hot springs of Costa Rica. Environ Microbiol 10: 460-473.
17. Flores, E., and Herrero, A. (2010) Compartmentalized function through cell differentiation in filamentous cyanobacteria. Nat Rev Microbiol 8: 39-50.
18. Flores, E., Pernil, R., Muro-Pastor, A.M., Mariscal, V., Maldener, I., Lechno-Yossef, S., etal. (2007) Septum-localized protein required for filament integrity and diazotrophy in the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 189: 3884-3890.
19. Fogg, G.E., Stewart, W.D.P., Fay, P., and Walsby, A.E. (1973) The Blue-Green Algae. London and New York: Academic Press.
20. Geitler, L. (1960) Schizophyzeen. Berlin-Nikolassee, Germany: Gebrüder Borntraeger.
21. Giddings, T.H.J., and Staehelin, L.A. (1978) Plasma membrane architecture of Anabaena cylindrica: occurrence of microplasmodesmata and changes associated with heterocyst development and the cell cycle. Cytobiologie 16: 235-249.
22. Giddings, T.H.J., and Staehelin, L.A. (1981) Observation of microplasmodesmata in both heterocyst-forming and non-heterocyst forming filamentous cyanobacteria by freeze-fracture electron microscopy. Arch Microbiol 129: 295-298.
23. Golubić, S., Hernandez-Marine, M., and Hoffmann, L. (1996) Developmental aspects of branching in filamentous Cyanophyta/Cyanobacteria. Arch Hydrobiol Suppl Algol Stud 83: 303-329.
24. Hernandez-Muniz, W., and Stevens, S.E.J. (1987) Characterization of the motile hormogonia of Mastigocladus laminosus. J Bacteriol 169: 218-223.
25. Kohl, F.G. (1903) Über die Organisation und Physiologic der Cyanophyeeenzelle und die mitotische Teilung ihres Kernes. Jena, Germany: Gustav Fischer.
26. Komárek, J., and Anagnostidis, K. (1989) Modern approach to the classification system of cyanophytes. 4-Nostocales. Algol Stud 56: 247-345.
27. Komárek, J., Kling, H., and Komárková, J. (2003) Filamentous cyanobacteria. In Freshwater Algae of North America. Wehr, J.D., and Sheath, R.G. (eds). San Diego, CA: Elsevier, pp. 117-196.
28. Konhauser, K.O., Lalonde, S.V., Planavsky, N.J., Pecoits, E., Lyons, T.W., Mojzsis, S.J., etal. (2011) Aerobic bacterial pyrite oxidation and acid rock drainage during the Great Oxidation Event. Nature 478: 369-373.
29. Lamont, H.C. (1969) Sacrificial cell death and trichome breakage in an Oscillatoriacean blue-green alga: the role of murein. Arch Microbiol 69: 237-259.
30. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., etal. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
31. Lehner, J., Berendt, S., Dörsam, B., Pérez, R., Forchhammer, K., and Maldener, I. (2013) Prokaryotic multicellularity: a nanopore array for bacterial cell communication. FASEB J 27: 1-8.
32. Lockau, W., and Ziegler, K. (2006) Cyanophycin inclusions: biosynthesis and applications. In Microbial Bionanotechnology: Biological Self-Assembly Systems and Biopolymer-Based Nanostructures. Rehm, B. (ed.). Norfolk, UK: Horizon Scientific Press, pp. 79-106.
33. Mackenzie, R., Pedrós-Alió, C., and Díez, B. (2013) Bacterial composition of microbial mats in hot springs in Northern Patagonia: variations with seasons and temperature. Extremophiles 17: 123-136.
34. Marcenko, E. (1962) Licht- und elektronenmikroskopische Untersuchungen an der Thermalalge Mastigocladus laminosus Cohn. Acta Bot Coratica 20/21: 47-74.
35. Mariscal, V., Herrero, A., Nenninger, A., Mullineaux, C.W., and Flores, E. (2011) Functional dissection of the three-domain SepJ protein joining the cells in cyanobacterial trichomes. Mol Microbiol 79: 1077-1088.
36. Markowitz, V.M., Chen, I.-M.A., Palaniappan, K., Chu, K., Szeto, E., Grechkin, Y., etal. (2012) IMG: the Integrated Microbial Genomes database and comparative analysis system. Nucleic Acids Res 40: D115-D122.
37. Martin, T.C., and Wyatt, J.T. (1974) Comparative physiology and morphology of six strains of Stigonematacean blue-green algae. J Phycol 10: 57-65.
38. Meeks, J.C., Campbell, E.L., Summers, M.L., and Wong, F.C. (2002) Cellular differentiation in the cyanobacterium Nostoc punctiforme. Arch Microbiol 178: 395-403.
39. Melick, D.R., Broady, P.A., and Rowan, K.S. (1991) Morphological and physiological characteristics of a non-heterocystous strain of the cyanobacterium Mastigocladus laminosus Cohn from fumarolic soil on Mt Erebus, Antarctica. Polar Biol 11: 81-89.
40. Merino-Puerto, V., Mariscal, V., Mullineaux, C.W., Herrero, A., and Flores, E. (2010) Fra proteins influencing filament integrity, diazotrophy and localization of septal protein SepJ in the heterocyst-forming cyanobacterium Anabaena sp. Mol Microbiol 75: 1159-1170.
41. Merino-Puerto, V., Schwarz, H., Maldener, I., Mariscal, V., Mullineaux, C.W., Herrero, A., and Flores, E. (2011) FraC/FraD-dependent intercellular molecular exchange in the filaments of a heterocyst-forming cyanobacterium, Anabaena sp. Mol Microbiol 82: 87-98.
42. Miller, S.R., Purugganan, M.D., and Curtis, S.E. (2006) Molecular population genetics and phenotypic diversification of two populations of the thermophilic cyanobacterium Mastigocladus laminosus. Appl Environ Microbiol 72: 2793-2800.
43. Morin, N., Vallaeys, T., Hendrickx, L., Natalie, L., and Wilmotte, A. (2010) An efficient DNA isolation protocol for filamentous cyanobacteria of the genus Arthrospira. J Microbiol Methods 80: 148-154.
44. Mullineaux, C.W., Mariscal, V., Nenninger, A., Khanum, H., Herrero, A., Flores, E., and Adams, D.G. (2008) Mechanism of intercellular molecular exchange in heterocyst-forming cyanobacteria. EMBO J 27: 1299-1308.
45. Nayar, A.S., Yamaura, H., Rajagopalan, R., Risser, D.D., and Callahan, S.M. (2007) FraG is necessary for filament integrity and heterocyst maturation in the cyanobacterium Anabaena sp. strain PCC 7120. Microbiology 153: 601-607.
46. Nierzwicki, S.A., Maratea, D., Balkwill, D.L., Hardie, L.P., Mehta, V.B., and Stevens, S.E.J. (1982) Ultrastructure of the cyanobacterium, Mastigocladus laminosus. Arch Microbiol 133: 11-19.
47. Nierzwicki-Bauer, S.A., Balkwill, D.L., and Stevens, S.E.J. (1984a) Heterocyst differentiation in the cyanobacterium Mastigocladus laminosus. J Bacteriol 157: 514-525.
48. Nierzwicki-Bauer, S.A., Balkwill, D.L., and Stevens, S.E.J. (1984b) Morphology and ultrastructure of the cyanobacterium Mastigocladus laminosus growing under nitrogen-fixing conditions. Arch Microbiol 137: 97-103.
49. Pankratz, H.S., and Bowen, C.C. (1963) Cytology of blue-green algae. I. The cells of Symploca muscorum. Am J Bot 50: 387-399.
50. Reynolds, E.S. (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17: 208-212.
51. Rippka, R., Deruelles, J., Waterbury, J.B., Herdman, M., and Stanier, R.Y. (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111: 1-61.
52. Robinson, W.B., Mealor, A.E., Stevens, S.E.J., and Ospeck, M. (2007) Measuring the force production of the hormogonia of Mastigocladus laminosus. Biophys J 93: 699-703.
53. Schirrmeister, B.E., Anisimova, M., Antonelli, A., and Bagheri, H.C. (2011) Taxa required for improved phylogenomic approaches. BMC Evol Biol 4: 424-427.
54. Schneider, D., Fuhrmann, E., Scholz, I., Hess, W.R., and Graumann, P.L. (2007) Fluorescence staining of live cyanobacterial cells suggest non-stringent chromosome segregation and absence of a connection between cytoplasmic and thylakoid membranes. BMC Cell Biol 10: 1-10.
55. Schwabe, G.H. (1960) Über den thermobionten Kosmopoliten Mastigocladus laminosus Cohn. Schweiz Z Hydrol 22: 759-792.
56. Shih, P.M., Wu, D., Latifi, A., Axen, S.D., Fewer, D.P., Talla, E., etal. (2013) Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc Natl Acad Sci USA 110: 1053-1058.
57. Singh, R.N., and Tiwari, D.N. (1969) Induction by ultraviolet irradiation of mutation in the blue-green alga Nostoc linckia (Roth) Born. et Flah. Nature 221: 62-64.
58. Smith, D.J., Timonen, H.J., Jaffe, D.A., Griffin, D.W., Birmele, M.N., Perry, K.D., etal. (2013) Intercontinental dispersal of bacteria and archaea by transpacific winds. Appl Environ Microbiol 79: 1134-1139.
59. Soe, K.M., Yokoyama, A., Yokoyama, J., and Hara, Y. (2011) Morphological and genetic diversity of the thermophilic cyanobacterium, Mastigocladus laminosus (Stigonematales, Cyanobacteria) from Japan and Myanmar. Phycol Res 59: 135-142.
60. Stevens, S.E.J., Nierzwicki-Bauer, S.A., and Balkwill, D.L. (1985) Effect of nitrogen starvation on the morphology and ultrastructure of the cyanobacterium Mastigocladus laminosus. J Bacteriol 161: 1215-1218.
61. Szklarczyk, R., and Heringa, J. (2004) Tracking repeats using significance and transitivity. Bioinformatics 20: 311-317.
62. Thurston, E.L., and Ingram, L.O. (1971) Morphology and fine structure of Fischerella ambigua. J Phycol 7: 203-210.
63. Tomitani, A., Knoll, A.H., Cavanaugh, C.M., and Ohno, T. (2006) The evolutionary diversification of cyanobacteria: molecular-phylogenetic and paleontological perspectives. Proc Natl Acad Sci USA 103: 5442-5447.
64. Wildon, D.C., and Mercer, F.V. (1963) The ultrastructure of the vegetative cell of blue-green algae. Aust J Biol Sci 16: 585-596.
65. Wilk, L., Strauss, M., Rudolf, M., Nicolaisen, K., Flores, E., Kühlbrandt, W., and Schleiff, E. (2011) Outer membrane continuity and septosome formation between vegetative cells in the filaments of Anabaena sp. PCC 7120. Cell Microbiol 49: 1-12.
66. Zhang, J.-Y., Chen, W.-L., and Zhang, C.-C. (2009) hetR and patS, two genes necessary for heterocyst pattern formation, are widespread in filamentous nonheterocyst-forming cyanobacteria. Microbiology 155: 1418-1426.