Comamonas testosteroni
Classification
Higher order taxa
Domain: Bacteria; Phylum: Pseudomonadota; Class: Betaproteobacteria; Order: Burkholderiales; Family: Comamonadaceae [1]
Species
Comamonas testosteroni
Description and significance
Comamonas testosteroni, previously known as Pseudomonas testosteroni [2], is a bacterium known for its ability to break down plastics. It is the most common of the four species within the Comamonas genus [3]. The bacterium's name derives from its capability to use testosterone as a carbon source [4]. C. testosteroni occupies a range of diverse habitats, from activated sludge to marine environments [5]. This bacterium is of importance to the public as it can break down harmful toxins found in wastewater, converting them into harmless chemicals in a process known as bioaugmentation [6]. However, C. testosteroni can also act as a human pathogen, posing a risk to immunocompromised individuals [7]. The plastic-degrading capabilities and bioaugmentation applications of C. testosteroni are not yet fully explored and remain ongoing fields of study [6].
Genome structure
The genome of C. testosteroni consists of one circular chromosome, with some strains harboring additional circular plasmids. Based on genomic data from fourteen different strains of C. testosteroni, the bacterium’s genome size ranges from 5,060,000 to 6,030,000 base pairs, with G + C content ranging from 61.1% to 61.8% [8]. Approximately 85% of the genome of C. testosteroni consists of coding sequences, with between 4674 and 5645 open reading frames that contain an average of 897 to 938 base pairs each [8]. Approximately 80% of these genes encode functional proteins [9]. Genetic analyses indicate that a substantial percentage of C. testosteroni genes are associated with transportation (22%) and signaling (6%), which indicates that C. testosteroni is able to adapt to a variety of environmental conditions. [5] Notably, the bacterium possesses a signaling system which allows it to switch between planktonic and biofilm lifestyles [9].
C. testosteroni lacks certain genes related to glycolysis which prevents it from consuming sugars other than glycerol and gluconate [5]. Specifically, the bacterium lacks two key components of the pentose phosphate pathway which renders it unable to oxidize glucose [5]. Instead, this bacterium possesses genes allowing it to consume aromatic compounds and fatty acids. Genes involved in degrading aromatic compounds include catechol and protocatechuate [5].
The pan-genome of C. testosteroni, which contains gene families found in all sequenced strains, is 2.8 times the size of the core genome, which only contains gene families shared by all sequenced strains. The pan-genome of this taxon is classified as open, meaning that sequencing new strains will continue to reveal unique gene families not found in other strains of C. testosteroni [8].
Cell structure
C. testosteroni is a member of the genus Comamonas, which is comprised of Gram-negative, aerobic, nonpigmented, bacilli (rod-shaped) bacterial species. These species, including C. testosteroni, possess tufts of polar or bipolar flagella which allow them to move through the environment [10]. Comamonas cells are 0.5 to 2 µm in width and 1 to 6 µm in length and are straight or slightly curved. Colonies of C. testosteroni are transparent, with smooth or granular surfaces, featuring round or wavy borders [10].
Metabolic processes
C. testosteroni is a Gram-negative bacterium that utilizes aerobic respiration [5]. C. testosteroni thrives in diverse environments due to its unique metabolic capabilities [11]. The bacterium metabolizes aromatic carbons, gluconeogenic substrates, various acids, and steroids like testosterone without competing with sugar-based carbon sources due to the absence of genes encoding glycolysis-related proteins [12]. C. testosteroni breaks down carboxylic acids into intermediates for cell growth via the tricarboxylic acid cycle [5] and metabolizes aromatic carbon compounds through the protocatechuate 4,5-cleavage pathway [11]. This mechanism allows C. testosteroni to compost plastics and other compounds that are toxic to humans, such as polycyclic aromatic hydrocarbons (PAHs) [11]. In addition to its preference for aromatic compounds and carboxylic acids, C. testosteroni metabolizes testosterone and other androgens in the environment using the 9,10-seco pathway [4]. C. testosteroni can also synthesize all cellular components by itself, including nucleotides, amino acids, and fatty acids [5].
Ecology
C. testosteroni lives either in planktonic form as free-living bacterial cells, or in biofilms (assemblies of bacterial cells which form a sheet-like coating on a given surface) [9]. The ability of C. testosteroni to form biofilms allows the bacteria to grow and survive under harsher conditions compared to bacteria living in planktonic form [9]. Because of this ability, C. testosteroni inhabits many different environments like activated sludge (sewage containing microorganisms), marshes, marine habitats, and animal tissues [5].
Pathology
Although C. testosteroni is not part of the typical human microbiome and possesses low virulence, it can cause infections, predominantly acquired from the community as opposed to from healthcare settings. As of 2022, there have been 51 reported cases of C. testosteroni infections, with 7 of these cases resulting in death [7]. C. testosteroni can act as a human pathogen in various healthcare settings, causing hospital-acquired (nosocomial) infections via intravenous and urinary catheters [7]. C. testosteroni can also cause mild, persistent intra-abdominal infections in immunocompromised individuals by directly invading tissues within the gastrointestinal tract [3]. C. testosteroni responds to various antibiotic treatments except in cases of nosocomial multidrug-resistant infections. Some of the antibiotics that have been known to treat C. testosteroni are Cefipime, Ciprofloxacin, Ampicillin, and Meropenem [7].
Bioaugmentation Applications
Bioaugmentation is the removal of undesirable compounds from hazardous waste using microorganisms. C. testosteroni has bioaugmentation properties since it breaks down substances such as 3-chloroaniline (3-CA), a toxic chemical to humans, into a harmless substance [6]. In addition, androgens, a class of steroid hormones, contaminate wastewater in sewage and can pose risks to human health. This bacterium breaks down androgens via aerobic degradation [12]. Furthermore, C. testosteroni accelerates the process of bioaugmentation by breaking down pyridine through mono-oxygenation reactions [13]. While C. testosteroni can effectively degrade these toxic compounds in activated sludge, the efficacy of its degradation decreases over time [6].
Current Research
Current research concerning C. testosteroni revolves around understanding the potential bioaugmentation applications of the microorganism. One study focuses on the role it plays in the degradation of pyridine, a wastewater pollutant [13]. The study involved acclimating sludge biomass from a wastewater treatment plant to a new environment by using glucose as the primary substrate, then gradually adding pyridine. C. testosteroni was then isolated based on its pyridine-degrading capabilities [13]. C. testosteroni aided in the removal of pyridine from wastewater, accelerated the mono-oxidation (degradation) of pyridine, and increased the speed of mineralization from toxic to innocuous substances. However, the addition of C. testosteroni in the biodegradation process had minimal effects on the microbial community as a whole [13].
Additional ongoing research investigates the ability of C. testosteroni to break down plastics, specifically, the genetic structure that is responsible for regulating this metabolism and how it can be used in a plastic-recycling setting. A recent study mapped the pathways activating this function in C. testosteroni [4]. This research found that the 4,5 meta reaction is the main pathway involved in the upregulation of aromatic carbon cleavage pathways that break down plastics [4].
References
1. Schoch, C.L. et al. (2020). NCBI Taxonomy: a comprehensive update on curation, resources and tools. Database (Oxford). https://doi.org/10.1093/database/baaa062
2. Steinberg, J.P., and E.M. Burd. (2015). 238 - other gram-negative and gram-variable bacilli. In Bennett, J.E., Dolin, R., and Blaser, M.J. (eds). Mandell, Douglas, and Bennett's principles and practice of infectious diseases (eighth edition). Philadelphia, PA. https://doi.org/10.1016/B978-1-4557-4801-3.00238-1
3. Farooq, S., R. Farooq, and N. Nahvi. (2017). Comamonas testosteroni: Is It Still a Rare Human Pathogen?. Case reports in gastroenterology, 11(1), 42–47. https://doi.org/10.1159/000452197
4. Wilkes, R.A., J. Waldbauer, A. Caroll, M. Nieto-Domínguez, D. J. Parker, L. Zhang, A.M. Guss, and L. Aristilde. (2023). Complex regulation in a Comamonas platform for diverse aromatic carbon metabolism. Nature Chemical Biology 19, 651–662. https://doi.org/10.1038/s41589-022-01237-7
5. Ma, Y., Y. Zhang, J. Zhang, D. Chen, Y. Zhu, H. Zheng, S. Wang, C. Jiang, G. Zhao, and S. Liu. (2009). The complete genome of Comamonas testosteroni reveals its genetic adaptations to changing environments. Applied and Environmental Microbiology 75(21), 6812-6819. https://doi.org/10.1128/AEM.00933-09
6. Boon, N., J. Goris, P. De Vos, W. Verstraete, and E.M. Top. (2000). Bioaugmentation of Activated Sludge by an Indigenous 3-Chloroaniline-Degrading Comamonas testosteroni Strain, I2gfp. Applied and Environmental Microbiology 66(7), 2906–2913. https://doi.org/10.1128/AEM.66.7.2906-2913.2000
7. Sammoni A., A. Abdalah, and M. Al-Aissami. (2022). Comamonas testosteroni bacteremia: A rare unusual pathogen detected in a burned patient: Case report and literature review. Annals of medicine and surgery 75, 103371. https://doi.org/10.1016/j.amsu.2022.103371
8. Liu, L., W. Zhu, Z. Cao, B. Xu,G. Wang, and M. Luo. (2015). High correlation between genotypes and phenotypes of environmental bacteria Comamonas testosteroni strains. BMC Genomics 16, 110. https://doi.org/10.1186/s12864-015-1314-x
9. Wu, Y., K. Arumugam, M.Q.X. Tay, H. Seshan, A. Mohanty, and B. Cao. (2015). Comparative genome analysis reveals genetic adaptation to versatile environmental conditions and importance of biofilm lifestyle in Comamonas testosteroni. Applied Microbiology and Biotechnology 99, 3519–3532. https://doi.org/10.1007/s00253-015-6519-z
10. Willems, A., and P. De Vos. (2006). Comamonas. In Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, KH., Stackebrandt, E. (eds). The Prokaryotes. Springer, New York, NY. https://doi-org.ezproxy.bu.edu/10.1007/0-387-30745-1_31
11. Jiang, F., Z. Jiang, J. Huang, P. Tang, J. Cui, W. Feng, C. Yu, C. Fu, and Q. Lu. (2023). Exploration of potential driving mechanisms of Comamonas testosteroni in polycyclic aromatic hydrocarbons degradation and remodelled bacterial community during co-composting. Journal of Hazardous Materials 458, 132032. https://doi.org/10.1016/j.jhazmat.2023.132032
12. Chen, Y. L., C. H. Wang, F. C. Yang, W. Ismail, P. H. Wang, C. J. Shih, Y. C. Wu, and Y. R. Chiang. (2016). Identification of Comamonas testosteroni as an androgen degrader in sewage. Scientific Reports 6, 35386. https://doi.org/10.1038/srep35386
13. Zhu, G., Y. Zhang, S. Chen, L. Wang, Z. Zhang, and B.E. Rittmann. (2021). How bioaugmentation with Comamonas testosteroni accelerates pyridine mono-oxygenation and mineralization. Environmental Research 193, 110553. https://doi.org/10.1016/j.envres.2020.110553
14. Agricultural Research Service (NRRL) Culture Collection (https://commons.wikimedia.org/wiki/File:Comamonas_testosteroni_NRRL_B-2611_2.jpg), Comamonas testosteroni NRRL B-2611 2, marked as public domain.
Edited by [Madison Kim, Alexandra Pastushan, Margaret Reilly, Sophia Souza, and Anna Wozniak], students of Jennifer Bhatnagar for [http://www.bu.edu/academics/cas/courses/cas-bi-311/ BI 311 General Microbiology], 2023, Boston University.
