Sphingobium yanoikuyae
1. Classification
a. Higher order taxa
Bacteria; Pseudomonadota; Alphaproteobacteria; Sphingomonadales; Sphingomonadaceae; Sphingobium [1]
Species
Sphingobium yanoikuyae
2. Description and significance
"Sphingobium yanoikuyae" is a species of bacterium that is Gram-negative, nonmotile, non-sporulating, and rod-shaped [2]. "S. yanoikuyae" can break down polyaromatic hydrocarbons (PAHs), pollutants that have accumulated in the environment due to human activity, and can regulate cadmium levels in soils. "Sphingobium yanoikuyae" has additionally been found as a human pathogen in three clinical cases [7][15][16]. While the capabilities regarding PAHS of "Sphingobium yanoikuyae" have been known for decades, recent research has focused on expanding knowledge on the limits and biochemical pathways of PAH degradation and the genes involved [8]. More recent research has also shifted from utilizing the ability of "S. yanoikuyae" to degrade pollutants in agricultural settings to utilizing it as a way to boost plant growth [13][22].
3. Genome structure
The whole genome of "Sphingobium yanoikuyae" has been sequenced using the 454 Life Sciences GS FLX system. The draft genome was 5,353,044 bases in length with a mean GC content of 64.3% [5]. The genome of strain SHJ showed a total of 5,402 genes, with 5,183 protein-encoding genes, 143 pseudogenes and 76 noncoding RNA genes. 44 of the protein coding genes were found to potentially be involved in polyarylates (aromatic polyester) hydrolysis. Additionally, a region with a size of 6.9 kb that has 7 open reading frames, located on the smaller plasmid (pSES189) of the two total plasmids, is assumed to be responsible for biodegradation of phthalate [6]. "S. yanoikuyae" has 37 genes encoding enzymes that degrade complex organic pollutants, including polycyclic aromatic hydrocarbons and toluene. These include enzymes like pyrone-4,6-decarboxylase hydrolase and carboxy-2-hydroxy muconic semialdehyde dehydrogenase, which are essential for degrading aromatic compounds. Additionally, enzymes like lactoylglutathione lyase and benzoate 1,2-dioxygenase enable the organism to cleave aromatic rings, a key step in processing persistent organic pollutants. "S. yanoikuyae" possesses enzymes like alcohol dehydrogenases and carbohydrate-related transport proteins, which facilitate the breakdown and utilization of various sugars and alcohols. This capability supports its adaptation to different carbon sources in the environment [4].
4. Cell structure
"Sphingobium yanoikuyae" is a gram negative, nonmotile, non sporulating aerobic rod-shaped bacterium. Its cell wall is characterized by a thin peptidoglycan layer surrounded by an outer membrane with glycosphingolipids instead of lipopolysaccharides which are typically a major component of an outer membrane [5]. Another notable feature of the cell wall is the presence of sphingolipids, characteristic of the Sphingomonadaceae family, which contribute to the structural stability of the membrane, along with multiple short pili (fimbriae).
5. Metabolic processes
"S. yanoikuyae" is a chemoorganoheterotroph that is most notable for its ability to utilize a variety of aromatic organic compounds such as biphenyl, naphthalene, phenanthrene, and toluene as its sole carbon source [8]. Additionally, some "S. yanoikuyae" can produce carotenoids, namely zeaxanthin, which the bacterium uses to modulate its membrane fluidity, enhance its ability to degrade heterocyclic compounds, and defend against intracellular oxidative stress [23].
Different strains of "S. yanoikuyae" isolated from different environments have variations in their specific degradation capabilities and genetic makeup, but generally share core characteristics, including lipases, dioxygenases, esterases, and dehydrogenases[4][9][10]. Different strains also exhibit varying metabolic capabilities, with some having a broader range of substrates for metabolism than others. For example, the B1 strain can degrade a wider range of aromatic hydrocarbons than strain TNE12. In a physiological and genetic comparison of the two strains, southern blots revealed significant homology, however certain genes responsible for monocyclic aromatics were missing in TNE12’s genome [11].
6. Ecology
"S. yanoikuyae" can survive in a wide range of habitats (including rhizospheres, contaminated soils, and deep ocean sediments) due to its ability to survive under low nutrient conditions and metabolize a variety of hydrocarbons including pollutants [12]. For studies done on "S. yanoikuyae", specimens were collected from soil in Mexico, Germany, Malaysia, India, China, and river water from Tokyo. The specimen was typically stored at a range of 23°C to 30°C and a pH of around 7, implying that the bacteria prefer warmer temperatures and neutral environments [3][4][10][12][13][14]. The bacterium has additionally been collected from tropical rainforests and sea-floor sediments, implying it prefers moist soils [13][10].
7. Bioremediation
Due to "S. yanoikuyae"’s ability to metabolize pollutants commonly found in soil, such as aromatic hydrocarbons, the bacterium has been a part of multi-disciplinary efforts to remediate contaminated soils. However, a recent study highlights challenges in using S.yanoikuyae as an inoculum for bioremediation. Contaminated soils naturally have populations of native bacteria that can degrade PAHs that can compete, which underscores the importance of considering niche competition and inocula survivability when designing bioremediation strategies [12].
8. Pathology
"S. yanoikuyae" can be a pathogen of humans. The first case reported of "S. yanoikuyae" behaving as a human pathogen was in 2021, when it infected the central nervous system of a 31-month-old male [15] "S. yanoikuyae" was found in the patients’ cerebral spinal fluid and the infection was treated with meropenem, an antibiotic, for 14 days and intrathecal amikacin treatment, another antibiotic, for 5 days [16]. A second case was reported in 2023, where "S. yanoikuyae" was found as the bacteria responsible for an infection in an 87-year-old patient who was receiving treatment via peritoneal dialysis for end-stage renal failure [15]. This patient was also treated with meropenem [16]. A third case of infection by "S. yanoikuyae" happened in May 2024, when an 89-year-old male had a case of "S. yanoikuyae" bacteremia [7]. This patient was treated with ceftriaxone and ceftazidime, two antibiotics, but ultimately died due to respiratory failure. [7] Doctors think he was prone to infection because he had been taking prednisolone for 6 years [7]. The mechanism by which "S. yanoikuyae" can behave as a pathogen is poorly understood.
Bacteria within the genus Sphingomonas have been found in medical devices such as respirators and dialysis equipment, and have been found to cause pneumonia, intravascular catheter-related infections, skin and soft tissue infections, urinary tract infections, and meningitis [15][16].
9. Current Research
While "Sphingobium yanoikuyae" was discovered in 1990, much of the research on this organism has happened in the last 7 years [17]. Of these recent papers, focus has been placed on identifying the degradative capabilities of this taxon. While "Sphingobium yanoikuyae"’s ability to degrade PAHs are known, the full scope of its degradative pathway and limitations are currently unknown [18]. Many studies have begun to investigate the bacteria’s catabolism of chemical compounds other than PAHs, such as ibuprofen and diethyl phthalates. Recently, it was discovered that "Sphingobium yanoikuyae" is also capable of breaking down these xenobiotics [2][3]. These findings led to the next group of more recent studies which focused on the use of "Sphingobium yanoikuyae" for bioremediation. One study looked at "Sphingobium yanoikuyae" activity in biochar and found that the bacteria significantly degrades PAH pollutants that were adsorbed on the biochar [19]. Another study looked at ibuprofen contamination in wetlands and discovered that the combination of the plant Phalaris arundinacea and "Sphingobium yanoikuyae" removes the ibuprofen from the soil [20]. The most recent group of studies looked at the above abilities of "Sphingobium yanoikuyae" and began contemplating the agricultural use of "Sphingobium yanoikuyae". A study showed that a Salix matsudana Koidz tree grown with "Sphingobium yanoikuyae" in the soil was better able to tolerate cadmium poisoning with the bacteria playing a role in regulating the toxic effects of cadmium [21]. In addition, the inoculation of the soil with "Sphingobium yanoikuyae" showed significant root growth and biomass production for both Oryza sativa (rice) and Capsicum chinense [13][22].
10. References
[1] [NCBI. (n.d.). Taxonomy Browser – "Sphingobium yanoikuyae". Retrieved October 15, 2024, from https://www.ncbi.nlm.nih.gov/Taxonomy/Browser/wwwtax.cgi?mode=Info&id=13690&lvl=3&lin=f&keep=1&srchmode=1&unlock]
[2] [Faisal, R. M., & Al-Shiti, A. Y. (2023). Characterization of a novel pathway for xanthene degradation by the engineered strain "Sphingobium yanoikuyae" B1DR. Baghdad Science Journal, 20(2), 0409. https://doi.org/10.21123/bsj.2022.6731 ]
[3] [Wang, Y., Liu, H., Peng, Y., Tong, L., Feng, L., & Ma, K. (2018). New pathways for the biodegradation of diethyl phthalate by "Sphingobium yanoikuyae" SHJ. Process Biochemistry, 71, 152–158. https://doi.org/10.1016/j.procbio.2018.05.010]
[4][ Lopez, E.S., Elufisan, T.O., Bustos, P., Charles, C.P.M., Mendoza-Herrera, A., & Guo, X. (2022). Complete Genome Report of a Hydrocarbon-Degrading "Sphingobium yanoikuyae" S72. Applied Sciences, 12(12), 6201. https://doi.org/10.3390/app12126201] [5][ Gai, Zhonghui, et al. Genome Sequence of "Sphingobium yanoikuyae" XLDN2-5, an Efficient Carbazole-Degrading Strain, Journal of Bacteriology, vol. 193, no. 22, 15 Nov. 2011, pp. 6404–6405, https://doi.org/10.1128/jb.06050-11.]
[6] [Feng, Liang, et al. Characterization and Genome Analysis of a Phthalate Esters-Degrading Strain "Sphingobium yanoikuyae" SHJ, BioMed Research International, vol. 2018, no. 3917054, 3 July 2018, pp. 1–8, pmc.ncbi.nlm.nih.gov/articles/PMC6051330/, https://doi.org/10.1155/2018/3917054.]
[7] [Miyamatsu, Y., Tanizaki, R., & Yamada, S. (2024). "Sphingobium yanoikuyae" Bacteremia, Japan. Emerging Infectious Diseases, 30(5), 1060-1062. https://doi.org/10.3201/eid3005.231514.]
[8] [G J Zylstra, E Kim, Aromatic hydrocarbon degradation by Sphingomonas yanoikuyae B1, Journal of Industrial Microbiology and Biotechnology, Volume 19, Issue 5-6, 1 November 1997, Pages 408–414, https://doi.org/10.1038/sj.jim.2900475]
[9] [Yin C, Xiong W, Qiu H, Peng W, Deng Z, Lin S, Liang R. Characterization of the Phenanthrene-Degrading "Sphingobium yanoikuyae" SJTF8 in Heavy Metal Co-Existing Liquid Medium and Analysis of Its Metabolic Pathway. Microorganisms. 2020 June 23;8(6):946. https://doi.org/10.3390/microorganisms8060946]
[10] [Gu, J.-G., Han, B., Duan, S., Zhao, Z., & Wang, Y. (2009). Degradation of the endocrine-disrupting dimethyl phthalate carboxylic ester by Sphingomonas yanoikuyae DOS01 isolated from the South China Sea and the biochemical pathway. International Biodeterioration & Biodegradation, 10.1016/j.ibiod.2008.12.004]
[11] [Shuttleworth KL, Sung J, Kim E, Cerniglia CE. Physiological and genetic comparison of two aromatic hydrocarbon-degrading Sphingomonas strains. Mol Cells. 2000 Apr 30;10(2):199-205. https://doi.org/10.1007/s10059-000-0199-x]
[12] [Cunliffe, M., & Kertesz, M. A. (2006). Effect of "Sphingobium yanoikuyae" B1 inoculation on bacterial community dynamics and polycyclic aromatic hydrocarbon degradation in aged and freshly PAH-contaminated soils. Environmental Pollution, 144(1), 228-237]
[13][Jou, Y.-T., Tarigan, E. J., Prayogo, C., Kobua, C. K., Weng, Y.-T., & Wang, Y.-M. (2022). Effects of "Sphingobium yanoikuyae" SJTF8 on rice (Oryza sativa) seed germination and Root Development. Agriculture, 12(11), 1890. https://doi.org/10.3390/agriculture12111890]
[14] [Kushwaha, M., Singh, D., Akhter, Y., & Chatterjee, S. (2024). Biodegradation of dep, DIBP, and BBP by a psychrotolerant "Sphingobium yanoikuyae" strain P4: Degradation potentiality and mechanism study. Archives of Microbiology, 206(6). https://doi.org/10.1007/s00203-024-03977-7]
[15] [Ozenen, G., Sahbudak Bal, Z., Bilen, N. M., Yildirim Arslan, S., Aydemir, S., Kurugol, Z., & Ozkinay, F. (2021). The first report of Sphingomonas yanoikuyae as a human pathogen in a child with a central nervous system infection. The Pediatric Infectious Disease Journal, 40(12), e490-e492. https://doi.org/10.1097/INF.0000000000003309]
[16][Mouradi, S., Motte, G., Torner, S., Lebugle, P., Petitboulanger, N., Bemmerzouk, A., & Charles, P. (2023). "Sphingobium yanoikuyae" peritonitis in peritoneal dialysis: a case report. Bulletin de La Dyalise à Domicile, 6(3), 123–127. https://doi.org/10.25796/bdd.v6i3.80703]
[17] [Yabuuchi, E., Yano, I., Oyaizu, H., Hashimoto, Y., Ezaki, T., & Yamamoto, H. (1990). Proposals of sphingomonas paucimobilis gen. nov. and comb. Nov., sphingomonas parapaucimobilis sp. nov., sphingomonas yanoikuyae sp. nov., sphingomonas adhaesiva sp. nov., sphingomonas capsulata comb, Nov., and two genospecies of the genus sphingomonas. Microbiology and Immunology, 34(2), 99–119. https://doi.org/10.1111/j.1348-0421.1990.tb00996.x]
[18][Khara, P., Roy, M., Chakraborty, J., Dutta, A., & Dutta, T. K. (2018). Characterization of a topologically unique oxygenase from Sphingobium sp.. PNB capable of catalyzing a broad spectrum of aromatics. Enzyme and Microbial Technology, 111, 74–80. https://doi.org/10.1016/j.enzmictec.2017.10.006]
[19] [Tao, J., Wu, W., Lin, D., & Yang, K. (2022). Microbial degradation of nondesorbable organic compounds on biochars by extracellular reactive oxygen species. Journal of Hazardous Materials, 439, 129625. https://doi.org/10.1016/j.jhazmat.2022.129625]
[20] [Balciunas, E. M., Kappelmeyer, U., Harms, H., & Heipieper, H. J. (2020). Increasing ibuprofen degradation in constructed wetlands by bioaugmentation with gravel containing biofilms of an ibuprofen‐degrading "Sphingobium yanoikuyae". Engineering in Life Sciences, 20(5–6), 160–167. https://doi.org/10.1002/elsc.201900097]
[21] [Zeng, X., Pang, L., Chen, Y., Kong, X., Chen, J., & Tian, X. (2020). Bacteria "Sphingobium yanoikuyae" SY310 enhances accumulation capacity and tolerance of cadmium in Salix Matsudana Koidz roots. Environmental Science and Pollution Research, 27(16), 19764–19773. https://doi.org/10.1007/s11356-020-08474-0]
[22] [Rincón-Molina, C. I., Martínez-Romero, E., Aguirre-Noyola, J. L., Manzano-Gómez, L. A., Zenteno-Rojas, A., Rogel, M. A., Rincón-Molina, F. A., Ruíz-Valdiviezo, V. M., & Rincón-Rosales, R. (2022). Bacterial community with plant growth-promoting potential associated to pioneer plants from an active Mexican volcanic complex. Microorganisms, 10(8), 1568. https://doi.org/10.3390/microorganisms10081568]
[23] [Liu X, Gai Z, Tao F, Tang H, Xu P. Carotenoids play a positive role in the degradation of heterocycles by "Sphingobium yanoikuyae". PLoS One. 2012;7(6):e39522. doi: 10.1371/journal.pone.0039522. Epub 2012 Jun 20. PMID: 22745775; PMCID: PMC3380023.]
Edited by [Jennifer Bhatnagar and Jordan Coccoluto], student of Jennifer Bhatnagar for BI 311 General Microbiology, 2020, Boston University
