Spiroplasma citri

Spiroplasma citri is a bacterium species and the causative agent of Citrus stubborn disease.[1]

Its genome has been partially sequenced.[2]

The restriction enzyme SciNI, with the cutting site 5' GCGC / 3' CGCG, can be found in S. citri.

Euscelis incisa can be used as a vector of the bacterium to experimentally infect white clover (Trifolium repens).[3]

S. citri is a partially sequenced, Gram-positive plant pathogenic mollicute which has a wide host range. [4]

Spiroplasma citri
Scientific classification
Domain:
Bacteria
Phylum:
Mycoplasmatota
Class:
Mollicutes
Order:
Mycoplasmatales
Family:
Mycoplasmataceae
Genus:
Spiroplasma
Species:
S. citri
Binomial name
Spiroplasma citri

Taxonomy and Phylogeny

S. citri is a bacteria that belongs to the kingdom Bacteria, phylum Tenericutes, class Mollicutes, order Entomoplasmatales, family Spiroplasmataceae, and genus Spiroplasma.[4] Members of the Mollicutes class, such as Spiroplasma, are characterized by their reduced genomes and lack of a conventional cell wall, which is a result of their adaptation to parasitic or symbiotic lifestyles.[5] Although Spiroplasma, Mycoplasma, and Phytoplasma are all under the Mollicutes class, the Spiroplasma genus demonstrates a closer genetic relationship to Mycoplasma, an animal genus causing disease, than to Phytoplasma, a plant-associated genus,[6] as only Spiroplasma and Mycoplasma can import sugars through the phosphotransferase system and make ATP via ATP synthase, and Spiroplasma genomes are 1 Mbp larger than Phytoplasma genomes.[7] Most mollicutes are obligate pathogens or symbionts forming complex relationships with their hosts.[8] Notably, Spiroplasma and Phytoplasma exhibit complex life cycles associated with both insect and plant hosts.[6] Spiroplasma transfers between plants and insects through feeding, reflecting its dependency on both host types for survival and spread.[9] This taxonomic affiliation places S. citri within the Citri-Chrysopicola-Mirum clade; relevant neighboring species within this genus include S. kunkelii, S. phoeniceum, S. eriocheiris, S. melliferum, and S. penaei, which infect a variety of hosts including specific species of corn, periwinkles, shrimps, crabs, and honeybees. [6]

Discovery and Isolation

Around 1915, “Washington” navel trees near Redlands, California, were the first to show symptoms of what is now known as Citrus Stubborn Disease.[10] The disease was then reported outside of California for the first time in the Mediterranean in 1928,[11] suggesting its wider geographical spread and impact on citrus production by that time. However, S. citri, the bacterium responsible for Citrus stubborn disease, was not cultured and identified until 1973, initially discovered in California.[9] This identification was made by J. M. Bové, P. Saglio, M. Lhospital, D. Lafléche, G. Dupont, J. G. Tully, and E. A. Freundt. This team of scientists aimed to find the root cause of citrus stubborn disease, responsible for stunting the growth of citrus plants. The research team focused on young citrus leaves from plants because they were more likely to transmit the disease.[12] To culture S. citri, the team used specialized nutrient-rich media that included horse serum or cholesterol, essential for growth, which mimicked the intracellular environment of the plant phloem, facilitating the growth of this bacterium. The cultures were maintained under anaerobic conditions to replicate the low-oxygen environment inside host issues.[12] To study S. citri, they grew this bacterium in culture and successfully isolated it as a pure culture. From there, the scientists learned the unique biochemical properties of S. citri and what characteristics distinguished it as its own species.[12]

Morphology

S. citri belongs to the Spiroplasma genus within the mollicutes class, which is composed of Gram-positive bacteria that lack a cell wall.[13] S. citri typically has a helical structure due to the arrangement of fibril and MreB filaments along its cytoskeleton.[14] In its helical form, S. citri moves in a corkscrew motion, which plays a significant role in cell division and elongation.[13] However, its alternate forms—spherical or ovoid shapes and branches, non-helical filaments—use intracellular fibril filaments for motility, compensating for the absence of flagella. These filaments create kinks in the cell body, allowing S. citri to move.[14] The sizes of these forms vary greatly: spherical shapes measure 100 to 240 nanometers wide, while helical and branched nonhelical filaments are about 120 nanometers wide, and 2-4 micrometers long, with the potential to reach 15 micrometers in later growth stages.[13] When cultured on agar, S. citricolonies are around 0.2 millimeters in width and display either a fried-egg-like or granular appearance.[13]

Metabolism and physiology

The metabolic pathways of S. citri allow it to survive and proliferate within citrus plants. The tricarboxylic acid cycle is missing from S. citri which means that this bacterium predominantly relies on glycolysis for ATP production.[15] S. citrihas a reduced genome and lacks various metabolic pathways which explains its heavy dependence on its hosts for nutrients, including amino acids, sugars, nucleotides, and vitamins.[16] It lacks a cell wall and is unable to make fatty acids. However, it can modify host-derived lipids for its membrane structure.[17] Like other Spiroplasma species, S. citri is an auxotroph for most of the necessary amino acids, meaning that it obtains them from the host.[18] Spiroplasmas in general are more metabolically flexible which allow them to easily adapt to different environments.[6] In the case of S. citri, this is typically inside an insect or plant phloem. S. citri has virulence factors involved in host tissue degradation and evasion of host immune responses.[19]

Genomics

S. citri's genomics, pieced together through shotgun and chromosome-specific libraries sequencing, reveal key features of its 1820 kbp chromosome.[7]

Sequencing

Although only 92% of the genome could be sequenced, scientists were able to uncover phage-related sequences, 69 transposase copies, and an almost complete terpenoid biosynthetic pathway.[7] Functional complementation and gene inactivation studies demonstrated that S. citri fructose consumption induces plant disease symptoms, and the ABC-type transporter solute binding protein is implicated in insect transmission.[7] The genome includes seven plasmids (10-14 copies/cell) containing proteins for DNA transfer.[7] However, gene decay, observed through shortened coding sequences and incomplete housekeeping genes, as well as repeated sequences, that prevent full chromosome sequencing, add some complexity. Despite these challenges, the S. citri's stable genome demonstrates its overall adaptability.

Ecology

The role of S. citri in its environment is related to how it interacts with host plants, insect vectors, and abiotic factors. This bacterium is mainly transmitted by leafhoppers, which spread it from infected to healthy citrus plants through feeding habits.[20] Young citrus plants are more susceptible to infection because they are more attractive to leafhoppers, whereas older plants become less appealing to these insects.[21] S. citri exploits the nutrients of host plants to survive and reproduce. It is primarily found in the plant phloem, a tissue that is particularly nutrient-rich because it is responsible for transportation of sugars.[20] S. citri thrives and spreads in hot, dry weather, making it commonly found in the United States, the Middle East, North Africa, Central America, New Zealand, and part of Western Europe, particularly France, Italy, and Spain. Notably, in California, major citrus plants like oranges, grapefruits, and tangelos suffer notable yield losses due to S. citri infection, impacting 5-10% of trees.[16]

Environmental Impact

S. citri causes citrus stubborn disease, a disease that reduces the yield and quality of our citrus fruits, which are excellent sources of vitamin C.[20] Though S. citri predominantly affects citrus plants, it also impacts other essential crops, including tomatoes, lettuce, and carrots,[20] which directly impacts the profitability of the agricultural industry and disrupts our food supply. It is important we further study this bacteria in order to learn how to effectively combat it, so that we can develop better management strategies to help minimize financial losses in the produce industry, and to reduce its impact on citrus production as well as on native plant species.

References

  1. ^ Spiroplasma citri gen. and sp. n.: A Mycoplasma-Like Organism Associated with “Stubborn” Disease of Citrus. P. Saglio, M. Lhospital, D. Laflèche, G. Dupont, J. M. Bové, J. G. Tully and E. A. Freundt, IJSEM, July 1973, volume 23, number 3, pages 191-204, doi:10.1099/00207713-23-3-191
  2. ^ Partial Chromosome Sequence of Spiroplasma citri Reveals Extensive Viral Invasion and Important Gene Decay. Patricia Carle, Colette Saillard, Nathalie Carrère, Sébastien Carrère, Sybille Duret, Sandrine Eveillard, Patrice Gaurivaud, Géraldine Gourgues, Jérome Gouzy, Pascal Salar, Eric Verdin, Marc Breton, Alain Blanchard, Frédéric Laigret, Joseph-Marie Bové, Joel Renaudin and Xavier Foissac, Appl. Environ. Microbiol., June 2010, volume 76, number 11, pages 3420-3426, doi:10.1128/AEM.02954-09
  3. ^ Spiroplasmas are the causal agents of citrus little-leaf disease. P. G. Markham, R. Townsend, M. Bar-Joseph, M. J. Daniels, A. Plaskitt and B. M. Meddins, Annals of Applied Biology, September 1974, Volume 78, Issue 1, pages 49–57, doi:10.1111/j.1744-7348.1974.tb01484.x
  4. ^ a b "Taxonomy browser (Spiroplasma citri)". www.ncbi.nlm.nih.gov. Retrieved 2024-05-06.
  5. ^ "Mollicutes: Molecular Biology and Pathogenesis". www.caister.com. Retrieved 2024-05-07.
  6. ^ a b c d Lo, Wen-Sui; Chen, Ling-Ling; Chung, Wan-Chia; Gasparich, Gail E.; Kuo, Chih-Horng (2013-01-16). "Comparative genome analysis of Spiroplasma melliferumIPMB4A, a honeybee-associated bacterium". BMC Genomics. 14 (1): 22. doi:10.1186/1471-2164-14-22. ISSN 1471-2164. PMC 3563533. PMID 23324436.
  7. ^ a b c d e Carle, Patricia; Saillard, Colette; Carrère, Nathalie; Carrère, Sébastien; Duret, Sybille; Eveillard, Sandrine; Gaurivaud, Patrice; Gourgues, Géraldine; Gouzy, Jérome; Salar, Pascal; Verdin, Eric; Breton, Marc; Blanchard, Alain; Laigret, Frédéric; Bové, Joseph-Marie (June 2010). "Partial Chromosome Sequence of Spiroplasma citri Reveals Extensive Viral Invasion and Important Gene Decay". Applied and Environmental Microbiology. 76 (11): 3420–3426. doi:10.1128/AEM.02954-09. ISSN 0099-2240. PMC 2876439. PMID 20363791.
  8. ^ Taylor, Mark; Mediannikov, Oleg; Raoult, Didier; Greub, Gilbert (February 2012). "Endosymbiotic bacteria associated with nematodes, ticks and amoebae" (PDF). FEMS Immunology & Medical Microbiology. 64 (1): 21–31. doi:10.1111/j.1574-695x.2011.00916.x. ISSN 0928-8244.
  9. ^ a b Cacciola, Santa Olga; Bertaccini, Assunta; Pane, Antonella; Furneri, Pio Maria (2017-04-12), "Spiroplasma spp.: A Plant, Arthropod, Animal and Human Pathogen", Citrus Pathology, IntechOpen, ISBN 978-953-51-3072-7, retrieved 2024-05-07
  10. ^ Gumpf, D. J. (1988), Maramorosch, Karl; Raychaudhuri, S. P. (eds.), "Stubborn Diseases of Citrus Caused by Spiroplasma Citri", Mycoplasma Diseases of Crops: Basic and Applied Aspects, New York, NY: Springer, pp. 327–342, doi:10.1007/978-1-4612-3808-9_17, ISBN 978-1-4612-3808-9, retrieved 2024-05-07
  11. ^ Bove, J. M.; Fos, A.; Lallemand, J. (June 1987). "Epidemiology of Spiroplasma citri in the Old World". Israel Journal of Medical Sciences. 23 (6): 663–666. ISSN 0021-2180. PMID 3312105.
  12. ^ a b c SAGLIO, P.; LHOSPITAL, M.; LAFLÈCHE, D.; DUPONT, G.; BOVÈ, J. M.; TULLY, J. G.; FREUNDT, E. A. (1973). "Spiroplasma citri gen. and sp. n.: A Mycoplasma-Like Organism Associated with "Stubborn" Disease of Citrus". International Journal of Systematic and Evolutionary Microbiology. 23 (3): 191–204. doi:10.1099/00207713-23-3-191. ISSN 1466-5034.
  13. ^ a b c d Cisak, Ewa; Wójcik-Fatla, Angelina; Zając, Violetta; Sawczyn, Anna; Sroka, Jacek; Dutkiewicz, Jacek (2015-12-13). "Spiroplasma – an emerging arthropod-borne pathogen?". Annals of Agricultural and Environmental Medicine. 22 (4): 589–593. doi:10.5604/12321966.1185758. ISSN 1232-1966. PMID 26706960.
  14. ^ a b Harne, Shrikant; Gayathri, Pananghat; Béven, Laure (2020). "Exploring Spiroplasma Biology: Opportunities and Challenges". Frontiers in Microbiology. 11. doi:10.3389/fmicb.2020.589279. ISSN 1664-302X. PMC 7609405. PMID 33193251.
  15. ^ Pollack, J. D.; McElwain, M. C.; DeSantis, D.; Manolukas, J. T.; Tully, J. G.; Chang, C.-J.; Whitcomb, R. F.; Hackett, K. J.; Williams, M. V. (1989). "Metabolism of Members of the Spiroplasmataceae". International Journal of Systematic and Evolutionary Microbiology. 39 (4): 406–412. doi:10.1099/00207713-39-4-406. ISSN 1466-5034.
  16. ^ a b McNeil, Christopher J.; Araujo, Karla; Godfrey, Kristine; Slupsky, Carolyn M. (February 2023). "Metabolite Signature and Differential Expression of Genes in Washington Navel Oranges ( Citrus sinensis ) Infected by Spiroplasma citri". Phytopathology. 113 (2): 299–308. doi:10.1094/PHYTO-05-22-0177-R. ISSN 0031-949X. PMID 35984373.
  17. ^ Freeman, B A; Sissenstein, R; McManus, T T; Woodward, J E; Lee, I M; Mudd, J B (March 1976). "Lipid composition and lipid metabolism of Spiroplasma citri". Journal of Bacteriology. 125 (3): 946–954. doi:10.1128/jb.125.3.946-954.1976. ISSN 0021-9193. PMC 236170. PMID 1254560.
  18. ^ Vera-Ponce León, Arturo; Dominguez-Mirazo, Marian; Bustamante-Brito, Rafael; Higareda-Alvear, Víctor; Rosenblueth, Mónica; Martínez-Romero, Esperanza (2021-04-06). "Functional genomics of a Spiroplasma associated with the carmine cochineals Dactylopius coccus and Dactylopius opuntiae". BMC Genomics. 22 (1): 240. doi:10.1186/s12864-021-07540-2. ISSN 1471-2164. PMC 8025503. PMID 33823812.
  19. ^ Bolaños, Luis M.; Servín-Garcidueñas, Luis E.; Martínez-Romero, Esperanza (2015-02-01). "Arthropod–Spiroplasma relationship in the genomic era". academic.oup.com. Retrieved 2024-05-07.
  20. ^ a b c d "Spiroplasma citri - an overview | ScienceDirect Topics". www.sciencedirect.com. Retrieved 2024-05-07.
  21. ^ "Spiroplasma citri (stubborn disease of citrus)". PlantwisePlus Knowledge Bank. Species Pages. 2022-01-07. doi:10.1079/pwkb.species.50977. ISSN 2958-4329.


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