Multiple Modes of Cell Death Discovered in a Prokaryotic (Cyanobacterial) Endosymbiont

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Zheng, Weiwen ^a,c   Rasmussen, Ulla ^b   Zheng, Siping ^c   Bao, Xiaodong ^d   Chen, Bin ^c   Gao, Yuan ^a   Guan, Xiong ^a   Larsson, John ^b   Bergman, Birgitta ^b  

^a FUJIAN AGRICULTURE AND FORESTRY UNIVERSITY   (China)

^b STOCKHOLM UNIVERSITY   (Sweden)

^c INSTITUTE OF PLANT PROTECTION   (China)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL MARKER; LIPOCORTIN 5; PEPTIDOGLYCAN; PHALLOIDIN;

ABIOTIC STRESS; APOPTOSIS; ARTICLE; AUTOPHAGY; BACTERIAL GENOME; CELL DEATH; CELL POPULATION; CELL TYPE; CELL WALL; CYANOBACTERIUM; CYTOSKELETON; DEVELOPMENTAL STAGE; ELECTRON MICROSCOPY; ENDOPHYTE; ENDOSYMBIONT; MICROSCOPY; NICK END LABELING; NONHUMAN; PROKARYOTIC CELL; SYMBIOSIS; TRANSMISSION ELECTRON MICROSCOPY; CYTOLOGY; FERN; MICROBIOLOGY; PHYSIOLOGY; PLANT LEAF;

AZOLLA FILICULOIDES; AZOLLA MICROPHYLLA; CYANOBACTERIA; EUKARYOTA; PROKARYOTA;

APOPTOSIS; CYANOBACTERIA; FERNS; PLANT LEAVES; SYMBIOSIS;

EID: 84879142241     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066147     Document Type: Article

References (46)

1. Melino G, Knight R, Nicotera P, (2005) How many ways to die? How many different models of cell death? Cell Death Differ 12: 1457-1462.
2. Vanlangenakker N, Berghe TV, Vandenabeele P, (2011) Many stimuli pull the necrotic trigger, an overview. Cell Death Differ 19: 75-86.
3. Denton D, Nicolson S, Kumar S, (2011) Cell death by autophagy: facts and apparent artefacts. Cell Death Differ 19: 87-95.
4. Bidle KD, Falkowski PG, (2004) Cell death in planktonic, photosynthetic microorganisms. Nat Rev Microbiol 2: 643-655.
5. Laporte C, Kosta A, Klein G, Aubry L, Lam D, et al. (2006) A necrotic cell death model in a protist. Cell Death Differ 14: 266-274.
6. Jiménez C, Capasso JM, Edelstein CL, Rivard CJ, Lucia S, et al. (2009) Different ways to die: cell death modes of the unicellular chlorophyte Dunaliella viridis exposed to various environmental stresses are mediated by the caspase-like activity DEVDase. J Exp Bot 60: 815-828.
7. Rice KC, Bayles KW, (2008) Molecular control of bacterial death and lysis. Microbiol Mol Biol Rev 72: 85-109.
8. Lewis K, (2000) Programmed death in bacteria. Microbiol Mol Biol Rev 64: 503-514.
9. Engelberg-Kulka H, Amitai S, Kolodkin-Gal I, Hazan R, (2006) Bacterial programmed cell death and multicellular behavior in bacteria. PLoS Genet 2: e135.
10. Uren AG, O'Rourke K, Aravind LA, Pisabarro MT, Seshagiri S, et al. (2000) Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol Cell 6: 961-967.
11. Asplund-Samuelsson J, Bergman B, Larsson J, (2012) Prokaryotic caspase homologs: phylogenetic patterns and functional characteristics reveal considerable diversity. PLoS One 7: e49888 doi:10.1371/journal.pone.0049888.
12. Schirrmeister BE, Antonelli A, Bagheri HC, (2011) The origin of multicellularity in cyanobacteria. BMC Evol Biol 11: 45 doi:10.1186/1471-2148-11-45.
13. Reyes-Prieto A, Bhattacharya D, (2007) Phylogeny of Calvin cycle enzymes supports Plantae monophyly. Mol Phylogenet Evol 45: 384-391 doi:10.1016/j.ympev.2007.02.026.
14. Falcón LI, Magallón S, Castillo A, (2010) Dating the cyanobacterial ancestor of the chloroplast. Isme J 4: 777-783 doi:10.1038/ismej.2010.2.
15. Usher KM, Bergman B, Raven JA, (2007) Exploring cyanobacterial mutualisms. Annu Rev Ecol Evol Syst 38: 255-273.
16. Peters GA, Meeks JC, (1989) The Azolla-Anabaena symbiosis: basic biology. Annu Rev Plant Physiol Plant Mol Biol 40: 193-210.
17. Zheng W, Rang L, Bergman B (2009) Structural characteristics of the cyanobacterium-Azolla symbioses. In: Pawlowski K, editor. Prokaryotic symbionts in plants. Springer. 235-263.
18. Ran L, Larsson J, Vigil-Stenman T, Nylander JAA, Ininbergs K, et al. (2010) Genome erosion in a nitrogen-fixing vertically transmitted endosymbiotic multicellular cyanobacterium. PLoS One 5: e11486 doi:10.1371/journal.pone.0011486.
19. Perkins S, Peters G, (1993) The Azolla-Anabaena symbiosis: endophyte continuity in the Azolla life-cycle is facilitated by epidermal trichomes†. New Phytol 123: 53-64.
20. Zheng W, Bergman B, Chen B, Zheng S, Guan X, et al. (2009) Cellular responses in the cyanobacterial symbiont during its vertical transfer between plant generations in the Azolla microphylla symbiosis. New Phytol 181: 53-61.
21. Ning S-B, Guo H-L, Wang L, Song Y-C, (2002) Salt stress induces programmed cell death in prokaryotic organism Anabaena. J Appl Microbiol 93: 15-28.
22. Berman-Frank I, Bidle KD, Haramaty L, Falkowski PG, (2004) The demise of the marine cyanobacterium, Trichodesmium spp., via an autocatalyzed cell death pathway. Limnol Ocean 49: 997-1005.
23. Galluzzi L, Aaronson SA, Abrams J, Alnemri ES, Andrews DW, et al. (2009) Guidelines for the use and interpretation of assays for monitoring cell death in higher eukaryotes. Cell Death Differ 16: 1093-1107 doi:10.1038/cdd.2009.44.
24. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, et al. (2009) Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 16: 3-11 doi:10.1038/cdd.2008.150.
25. Tang YZ, Dobbs FC, (2007) Green autofluorescence in dinoflagellates, diatoms, and other microalgae and its implications for vital staining and morphological studies. Appl Environ Microbiol 73: 2306-2313 doi:-10.1128/AEM.01741-06.
26. Van Heerde WL, Robert-Offerman S, Dumont E, Hofstra L, Doevendans PA, et al. (2000) Markers of apoptosis in cardiovascular tissues: focus on Annexin V. Cardiovasc Res. 45: 549-559.
27. Guljamow A, Delissen F, Baumann O, Thünemann AF, Dittmann E, (2012) Unique properties of eukaryote-type actin and profilin horizontally transferred to cyanobacteria. PLoS One 7: e29926 doi:10.1371/journal.pone.0029926.
28. Grasl-Kraupp B, Ruttkay-Nedecky B, Koudelka H, Bukowska K, Bursch W, et al. (1995) In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: a cautionary note. Hepatol Baltim Md 21: 1465-1468.
29. Tsiatsiani L, Van Breusegem F, Gallois P, Zavialov A, Lam E, et al. (2011) Metacaspases. Cell Death Differ 18: 1279-1288 doi:10.1038/cdd.2011.66.
30. Jiang Q, Qin S, Wu Q-Y, (2010) Genome-wide comparative analysis of metacaspases in unicellular and filamentous cyanobacteria. BMC Genomics 11: 198 doi:10.1186/1471-2164-11-198.
31. Vernet T, Khouri HE, Laflamme P, Tessier DC, Musil R, et al. (1991) Processing of the papain precursor. Purification of the zymogen and characterization of its mechanism of processing. J Biol Chem 266: 21451-21457.
32. Qu X, Zou Z, Sun Q, Luby-Phelps K, Cheng P, et al. (2007) Autophagy gene-dependent clearance of apoptotic cells during embryonic development. Cell 128: 931-946 doi:10.1016/j.cell.2006.12.044.
33. Erwig L-P, Henson PM, (2008) Clearance of apoptotic cells by phagocytes. Cell Death Differ 15: 243-250 doi:10.1038/sj.cdd.4402184.
34. Van Doorn WG, Beers EP, Dangl JL, Franklin-Tong VE, Gallois P, et al. (2011) Morphological classification of plant cell deaths. Cell Death Differ 18: 1241-1246 doi:10.1038/cdd.2011.36.
35. Smertenko A, Franklin-Tong VE, (2011) Organisation and regulation of the cytoskeleton in plant programmed cell death. Cell Death Differ 18: 1263-1270 doi:10.1038/cdd.2011.39.
36. Bursch W, Hochegger K, Torok L, Marian B, Ellinger A, et al. (2000) Autophagic and apoptotic types of programmed cell death exhibit different fates of cytoskeletal filaments. J Cell Sci 113 (Pt 7): 1189-1198.
37. Thorburn A, (2008) Apoptosis and autophagy: regulatory connections between two supposedly different processes. Apoptosis Int J Program Cell Death 13: 1-9 doi:10.1007/s10495-007-0154-9.
38. Gump JM, Thorburn A, (2011) Autophagy and apoptosis: what is the connection? Trends Cell Biol 21: 387-392 doi:10.1016/j.tcb.2011.03.007.
39. Reape TJ, Molony EM, McCabe PF, (2008) Programmed cell death in plants: distinguishing between different modes. J Exp Bot 59: 435-444 doi:10.1093/jxb/erm258.
40. Larsson J, Nylander JA, Bergman B, (2011) Genome fluctuations in cyanobacteria reflect evolutionary, developmental and adaptive traits. BMC Evol Biol 11: 187 doi:10.1186/1471-2148-11-187.
41. Ekman M, Tollbäck P, Bergman B, (2008) Proteomic analysis of the cyanobacterium of the Azolla symbiosis: identity, adaptation, and NifH modification. J Exp Bot 59: 1023-1034 doi:10.1093/jxb/erm282.
42. Deusch O, Landan G, Roettger M, Gruenheit N, Kowallik KV, et al. (2008) Genes of cyanobacterial origin in plant nuclear genomes point to a heterocyst-forming plastid ancestor. Mol Biol Evol 25: 748-761 doi:10.1093/molbev/msn022.
43. Brindefalk B, Ettema TJG, Viklund J, Thollesson M, Andersson SGE, (2011) A phylometagenomic exploration of oceanic alphaproteobacteria reveals mitochondrial relatives unrelated to the SAR11 clade. PLoS One 6: e24457 doi:10.1371/journal.pone.0024457.
44. Watanabe I, Espinas C, Berja N, Alimagno B (1977) The utilization of the Azolla-Anabaena complex as a nitrogen fertilizer for rice.
45. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797 doi:10.1093/nar/gkh340.
46. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ, (2009) Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinforma Oxf Engl 25: 1189-1191 doi:10.1093/bioinformatics/btp033.