International Journal of Molecular Sciences Review Chemotaxis Towards Aromatic Compounds: Insights from Comamonas testosteroni Yun-Hao Wang 1,2, Zhou Huang 1 and Shuang-Jiang Liu 1,2,* 1 State Key Laboratory of Microbial Resources and Environmental Microbiology Research Center, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China; [email protected] (Y.-H.W.); [email protected] (Z.H.) 2 University of Chinese Academy of Sciences, Beijing 101408, China * Correspondence: [email protected]; Tel.: +86-10-64807423 Received: 21 April 2019; Accepted: 30 May 2019; Published: 1 June 2019 Abstract: Chemotaxis is an important physiological adaptation that allows many motile bacteria to orientate themselves for better niche adaptation. Chemotaxis is best understood in Escherichia coli. Other representative bacteria, such as Rhodobacter sphaeroides, Pseudomonas species, Helicobacter pylori, and Bacillus subtilis, also have been deeply studied and systemically summarized. These bacteria belong to α-, γ-, "-Proteobacteria, or Firmicutes. However, β-Proteobacteria, of which many members have been identified as holding chemotactic pathways, lack a summary of chemotaxis. Comamonas testosteroni, belonging to β-Proteobacteria, grows with and chemotactically responds to a range of aromatic compounds. This paper summarizes the latest research on chemotaxis towards aromatic compounds, mainly from investigations of C. testosteroni and other Comamonas species. Keywords: Comamonas testosteroni; chemoreceptor; chemotaxis; aromatic compounds 1. Introduction Aromatic compounds have one or more aromatic rings containing resonance bonds, which make them chemically inert due to charge distribution over the whole skeleton of the aromatic ring. It has been estimated that about 25% of photosynthetic products from plants are deposited as lignin, which is one of the most abundant aromatic compounds on earth [1,2]. Other biogenic aromatic compounds, such as phenylalanine, tyrosine, tryptophan, many hormones, and signal molecules, play important roles in the maintenance and regulation of biological processes. Chemically synthesized aromatic compounds are important raw materials. Benzene, phenol, and toluene are classified as priority pollutants [3]. The toxicity and mutagenicity of nitroaromatic compounds have been documented [4,5]. Microbial biodegradation is an important process for removal of aromatic pollutants from environments [6,7]. In addition to metabolic robustness, microbial degradation also relies on the bioavailability of aromatic pollutants. Bacterial chemotactic responses toward aromatic compounds have attracted extensive interest [8–10] and are beneficial for bacteria to find more friendly environments and to degrade pollutants [11–13]. Chemotaxis may also facilitate the transfer of catabolic genes via motile bacteria to contaminated environments [14], thus promoting the coexistence of biodegradation and chemotaxis genes. Reviews are available on bacterial chemotaxis regarding stimulus-sensing and signal-processing [15], on exploring the function of bacterial chemotaxis [16], and on Pseudomonas chemotaxis [17]. This review is focused on the recent progress made on the study of bacterial chemotaxis towards aromatic compounds, in particular with Comamonas testosteroni. Int. J. Mol. Sci. 2019, 20, 2701; doi:10.3390/ijms20112701 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2019, 20, 2701 2 of 13 Int. J. Mol. Sci. 2019, 20, x FOR PEER REVIEW 2 of 13 2. The Taxonomy, Ecology, Physiology, and Chemotaxis of C. testosteroni C.C. testosteronitestosteronibelongs belongs tothe to genus theComamonas genus thatComamonas has 21 speciesthat (http:has //www.bacterio.21 species net(http://www.bacterio.net/comamonas.html)/comamonas.html) (Figure1). The Comamonas (Figure 1).species The Comamonas are Gram-negative species are bacteria Gram-negative belong tobacteriaβ-Proteobacteria, belong to β-Proteobacteria, and are distributed and are widely distributed in soil, widely sediments, in soil, sediments, and garden and ponds garden [18 ponds–20]. Based[18–20]. on Based the IMG on the database IMG database (https:// (https://img.jgi.doe.gov/),img.jgi.doe.gov/), 11 of the 11 21of theComamonas 21 Comamonasspecies species have beenhave genome-sequencedbeen genome-sequenced [21], [21], and and mining mining these these genomes genomes indicated indicated that that the the key key genes genes forfor hexosehexose phosphorylationphosphorylation werewere missingmissing [[22].22]. Thus, Thus, unlike unlike Pseudomonas species that prefer toto assimilateassimilate carbohydratescarbohydrates for growth, growth, the the ComamonasComamonas speciesspecies do do not not use use glucose glucose as a as sole a sole carbon carbon source, source, but butgrow grow well wellwith withnon-sugar non-sugar carbon carbon sources sources such as suchorganic as acids organic and acids aromatic and compounds. aromatic compounds. Although AlthoughComamonasComamonas and Pseudomonasand Pseudomonas species arespecies different are diinff erentcarbohydrate in carbohydrate assimilation, assimilation, they share they similar share similarecological ecological habitats, habitats, and both andare able both to are metabolize able to metabolizearomatic compounds. aromatic compounds. Studies have demonstrated Studies have demonstratedthat Comamonas that speciesComamonas playspecies an important play an important role in rolethe inbiological the biological geocycling geocycling of nutrients of nutrients in inenvironments environments [23–25], [23–25 ],as as well well as as in in bioremediation bioremediation of of polluted polluted environments environments [26–28]. [26–28]. A search onon WebWeb ofof ScienceScience using the key key word word “ “ComamonasComamonas”” revealed revealed more more than than 1700 1700 publications publications from from 2000 2000 to to2018, 2018, and and citation citation of ofthese these publication publication has has increased increased sharply sharply in in recent recent years, which suggests aa growinggrowing interestinterest fromfrom scientists.scientists. The C. testosteroni strainstrain CNB-1CNB-1 waswas isolatedisolated fromfrom activatedactivated sludgesludge andand growsgrows usingusing chloronitrobenzene chloronitrobenzene as as carbon carbon and and nitrogen nitrogen sources sources [29 [29];]; it has it has been been exploited exploited for thefor bioremediationthe bioremediation of chloronitrobenzene-polluted of chloronitrobenzene-polluted soil soil [30 ].[30]. The The genes genes involved involved in thein the degradation degradation of chloronitrobenezeof chloronitrobeneze were were located located on on a mega-plasmida mega-plasmid pCNB1 pCNB1 [31 [31],], and and the the degradation degradation pathwaypathway waswas identifiedidentified [[32].32]. Another strain ofof C. testosteroni,, CNB-2,CNB-2, isis aa derivativederivative fromfrom strainstrain CNB-1CNB-1 fromfrom whichwhich pCNB1pCNB1 waswas curedcured [[33].33]. FigureFigure 1.1. The genusgenus ComamonasComamonas:: phylogeny,phylogeny, diversity,diversity, habitats,habitats, andand genomes.genomes. TheThe phylogeneticphylogenetic analysisanalysis isis based based on on 16S 16S rRNA rRNA genes. genes. Background Background colors colors represent represent the origins the origins of type of strains type ofstrains species. of Thespecies. completeness The completeness of genomes of isgenomes indicated is byindicated circles outsideby circles the outside species the names. speciesComamonas names. Comamonas testosteroni istestosteroni indicated is by indicated an asterisk by (*).an asterisk (*). Bacterial chemotaxis is the movement of cells with either flagella, pili, or gliding structures in Bacterial chemotaxis is the movement of cells with either flagella, pili, or gliding structures in response to chemical gradients. The well-studied enteric Escherichia coli has only one gene cluster and response to chemical gradients. The well-studied enteric Escherichia coli has only one gene cluster and five chemoreceptors for chemotaxis. However, many environmental bacteria have more gene clusters and chemoreceptors. Studies show that the number of chemoreceptors in genomes is relevant to lifestyles, but not to genome sizes [34]. C. testosteroni strain CNB-1 is motile with 1–3 polar flagella Int. J. Mol. Sci. 2019, 20, 2701 3 of 13 five chemoreceptors for chemotaxis. However, many environmental bacteria have more gene clusters and chemoreceptors. Studies show that the number of chemoreceptors in genomes is relevant to lifestyles, but not to genome sizes [34]. C. testosteroni strain CNB-1 is motile with 1–3 polar flagella and chemotactically responds to a range of aromatic and other organic compounds (Table1). In contrast to E. coli, data-mining of the CNB-1 strain genome revealed two chemotaxis-like gene clusters and 19 putative chemoreceptor genes. Table 1. Summary of the chemotactic responses of Comamonas species to various organic compounds. Strain Potential Chemoeffector Refs Comamonas sp. strain JS765 2-nitrotoluene [35] benzoate 2-hydroxybenzoate 3-hydroxybenzoate 4-hydroxybenzoate 2,6-dihydroxybenzoate protocatechuate vanillic acid vanillin gallic acid gentisate Comamonas testosteroni phenol catechol [36–38] strain CNB-1 adipate succinate fumarate pyruvate citrate malate α-ketoglutarate cis-aconitate oxaloacetate isocitrate 1-dehydrotestosterone pregnenolone 17α-hydroxyprogesterone androstanedione Comamonas testosteroni 11α-hydroxyprogesterone testosterone [39] ATCC 11996 21α-hydroxyprogesterone