Lactonase

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acyl-L-homoserine-lactone lactonohydrolase
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EC no. 3.1.1.81
CAS no. 389867-43-0
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General chemical structure of an N-acyl homoserine lactone N-Acyl Homoserine Lactone.svg
General chemical structure of an N-acyl homoserine lactone

Lactonase (EC 3.1.1.81, acyl-homoserine lactonase; systematic name N-acyl-L-homoserine-lactone lactonohydrolase) is a metalloenzyme, produced by certain species of bacteria, which targets and inactivates acylated homoserine lactones (AHLs). It catalyzes the reaction

Contents

an N-acyl-L-homoserine lactone + H2O an N-acyl-L-homoserine

Many species of α-, β-, and γ-proteobacteria produce acylated homoserine lactones, small hormone-like molecules commonly used as communication signals between bacterial cells in a population to regulate certain gene expression and phenotypic behaviours. [1] This type of gene regulation is known as quorum sensing.

Other names for these types of enzymes are Quorum-quenching N-acyl-homoserine lactonase, acyl homoserine degrading enzyme, acyl-homoserine lactone acylase, AHL lactonase, AHL-degrading enzyme, AHL-inactivating enzyme, AHLase, AhlD, AhlK, AiiA, AiiA lactonase, AiiA-like protein, AiiB, AiiC, AttM, delactonase, lactonase-like enzyme, N-acyl homoserine lactonase, N-acyl homoserine lactone hydrolase, N-acyl-homoserine lactone lactonase, N-acyl-L-homoserine lactone hydrolase, quorum-quenching lactonase, quorum-quenching N-acyl homoserine lactone hydrolase. [2] [3] [4] [5] [6] [7] [8] [9] [10] [11] [12]

Enzyme mechanism

Lactonase hydrolyzes the ester bond of the homoserine lactone ring of acylated homoserine lactones. In hydrolysing the lactone bond, lactonase prevents these signaling molecules from binding to their target transcriptional regulators, thus inhibiting quorum sensing. [13]

Enzyme Structure

A dinuclear zinc binding site is conserved in all known lactonases and essential for enzyme activity and protein folding. [14]

Zn1 is tetracoordinated by His104, His106, His169, and the bridging hydroxide ion. Zn2 has five ligands, including Asp191, His235, His109, Asp108, and the bridging hydroxide ion. The metal ions assist in polarizing the lactone bond, increasing the electrophilicity of the lactone ring’s carbonyl carbon. Isotopic labeling studies indicated that the ring opening occurs via an addition elimination reaction with water addition shown below. [15]

Biological Function

Lactonases are able to interfere with AHL-mediated quorum sensing. Some examples of these lactonases are AiiA produced by Bacillus species, AttM and AiiB produced by Agrobacterium tumefaciens, and QIcA produced by Hyphomicrobiales species. [16]

Lactonases have been reported for Bacillus, Agrobacterium, Rhodococcus, Streptomyces, Arthrobacter, Pseudomonas, and Klebsiella. [17] The Bacillus cereus group (consisting of B. cereus, B. thuringiensis, B. mycoides, and B. anthracis) was found to contain nine genes homologous to the AiiA gene that encode AHL-inactivating enzymes, with the catalytic zinc-binding motif conserved in all cases. [18]

In the phytopathogen A. tumefaciens, AiiB lactonase acts as a fine modulator that essentially delays the release of lactone OC8-HSL and the resultant number of tumors produced by the pathogen. AttM lactonase mediates the degradation of the lactone OC8-HSL in wounded plant tissues. [19]

The primary activity of the anti-atherosclerotic paraoxonase (PON) enzymes is as lactonase. [20] Oxidized polyunsaturated fatty acids (notably in oxidized low-density lipoprotein) form lactone-like structures that are PON substrates. [20]

Ecology

It is still unclear the ecological effects of lactonase but it has been proposed that since bacteria mostly coexist with other microorganisms in the environment, some bacteria strains could have evolved its feeding strategies and utilize AHLs as their main resource for energy and nitrogen. [21]

Applications

Understanding the mechanisms and purposes of lactonase activity could lead to potential applied roles for these lactonases to control bacterial infections by inhibiting quorum-sensing activity and bring about profound effects on human health and the environment. However, in both the chemical and enzymatic lactonolysis, the reaction is reversible, complicating direct therapeutic application of lactonases. [22]

Pseudomonas aeruginosa , is an AHL-producing bacteria an opportunistic pathogen that infects immuno-compromised patients, [23] and is found in lung infections of cystic fibrosis patients. P. aeruginosa relies on quorum sensing via production of lactones N-butanoyl-L-homoserine (C4-HSL) and N-(3-oxododecanoyl)-l-HSL (3-oxo-C12-HSL) to regulate swarming, toxin and protease production, and proper biofilm formation. The absence of one or more components of the quorum-sensing system results in a significant reduction in virulence of the pathogen. [24]

Erwinia carotovora is a plant pathogen that causes soft rot in a number of crops such as potatoes and carrots [25] by using N-hexanoyl-l-HSL (C6-HSL) quorum sensing to evade the plant's defense systems and coordinate its production of pectate lyase during the infection process. [26]

Plants expressing AHL-Lactonase were shown to demonstrate enhanced resistance to infection from the pathogen Erwinia carotovora. Expression of virulence genes in E. Carotovora is regulated by N-(3-oxohexanoyl)-L-homoserine lactone (OHHL). Presumably, OHHL-hydrolysis via lactonase reduced OHHL levels, inhibiting the quorum-sensing systems driving virulence gene expression. [18]

See also

Related Research Articles

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<i>Bacillus cereus</i> Species of bacterium

Bacillus cereus is a Gram-positive rod-shaped bacterium commonly found in soil, food, and marine sponges. The specific name, cereus, meaning "waxy" in Latin, refers to the appearance of colonies grown on blood agar. Some strains are harmful to humans and cause foodborne illness due to their spore-forming nature, while other strains can be beneficial as probiotics for animals, and even exhibit mutualism with certain plants. B. cereus bacteria may be anaerobes or facultative anaerobes, and like other members of the genus Bacillus, can produce protective endospores. They have a wide range of virulence factors, including phospholipase C, cereulide, sphingomyelinase, metalloproteases, and cytotoxin K, many of which are regulated via quorum sensing. B. cereus strains exhibit flagellar motility.

In biology, quorum sensing or quorum signaling (QS) is the ability to detect and respond to cell population density by gene regulation. Quorum sensing is a type of cellular signaling, and more specifically can be considered a type of paracrine signaling. However, it also contains traits of both autocrine signaling: a cell produces both the autoinducer molecule and the receptor for the autoinducer. As one example, QS enables bacteria to restrict the expression of specific genes to the high cell densities at which the resulting phenotypes will be most beneficial, especially for phenotypes that would be ineffective at low cell densities and therefore too energetically costly to express. Many species of bacteria use quorum sensing to coordinate gene expression according to the density of their local population. In a similar fashion, some social insects use quorum sensing to determine where to nest. Quorum sensing in pathogenic bacteria activates host immune signaling and prolongs host survival, by limiting the bacterial intake of nutrients, such as tryptophan, which further is converted to serotonin. As such, quorum sensing allows a commensal interaction between host and pathogenic bacteria. Quorum sensing may also be useful for cancer cell communications.

<i>Aliivibrio fischeri</i> Species of bacterium

Aliivibrio fischeri is a Gram-negative, rod-shaped bacterium found globally in marine environments. This species has bioluminescent properties, and is found predominantly in symbiosis with various marine animals, such as the Hawaiian bobtail squid. It is heterotrophic, oxidase-positive, and motile by means of a single polar flagella. Free-living A. fischeri cells survive on decaying organic matter. The bacterium is a key research organism for examination of microbial bioluminescence, quorum sensing, and bacterial-animal symbiosis. It is named after Bernhard Fischer, a German microbiologist.

<i>N</i>-Acyl homoserine lactone Class of chemical compounds

N-Acyl homoserine lactones are a class of signaling molecules involved in bacterial quorum sensing, a means of communication between bacteria enabling behaviors based on population density.

<i>Pseudomonas aeruginosa</i> Species of bacterium

Pseudomonas aeruginosa is a common encapsulated, Gram-negative, aerobic–facultatively anaerobic, rod-shaped bacterium that can cause disease in plants and animals, including humans. A species of considerable medical importance, P. aeruginosa is a multidrug resistant pathogen recognized for its ubiquity, its intrinsically advanced antibiotic resistance mechanisms, and its association with serious illnesses – hospital-acquired infections such as ventilator-associated pneumonia and various sepsis syndromes.

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<i>Pseudomonas savastanoi</i> Species of bacterium

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<i>Pantoea</i> Genus of bacteria

Pantoea is a genus of Gram-negative bacteria of the family Erwiniaceae, recently separated from the genus Enterobacter. This genus includes at least 20 species. Pantoea bacteria are yellow pigmented, ferment lactose, are motile, and form mucoid colonies. Some species show quorum sensing ability that could drive different gene expression, hence controlling certain physiological activities. Levan polysaccharide produced by Pantoea agglomerans ZMR7 was reported to decrease the viability of rhabdomyosarcoma (RD) and breast cancer (MDA) cells compared with untreated cancer cells. In addition, it has high antiparasitic activity against the promastigote of Leishmania tropica.

<span class="mw-page-title-main">CsrB/RsmB RNA family</span> Non-coding RNA molecule

The CsrB RNA is a non-coding RNA that binds to approximately 9 to 10 dimers of the CsrA protein. The CsrB RNAs contain a conserved motif CAGGXXG that is found in up to 18 copies and has been suggested to bind CsrA. The Csr regulatory system has a strong negative regulatory effect on glycogen biosynthesis, glyconeogenesis and glycogen catabolism and a positive regulatory effect on glycolysis. In other bacteria such as Erwinia carotovora the RsmA protein has been shown to regulate the production of virulence determinants, such extracellular enzymes. RsmA binds to RsmB regulatory RNA which is also a member of this family.

Autoinducers are signaling molecules that are produced in response to changes in cell-population density. As the density of quorum sensing bacterial cells increases so does the concentration of the autoinducer. Detection of signal molecules by bacteria acts as stimulation which leads to altered gene expression once the minimal threshold is reached. Quorum sensing is a phenomenon that allows both Gram-negative and Gram-positive bacteria to sense one another and to regulate a wide variety of physiological activities. Such activities include symbiosis, virulence, motility, antibiotic production, and biofilm formation. Autoinducers come in a number of different forms depending on the species, but the effect that they have is similar in many cases. Autoinducers allow bacteria to communicate both within and between different species. This communication alters gene expression and allows bacteria to mount coordinated responses to their environments, in a manner that is comparable to behavior and signaling in higher organisms. Not surprisingly, it has been suggested that quorum sensing may have been an important evolutionary milestone that ultimately gave rise to multicellular life forms.

<i>Bacillus anthracis</i> Species of bacterium

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<span class="mw-page-title-main">LuxR-type DNA-binding HTH domain</span>

In molecular biology, the LuxR-type DNA-binding HTH domain is a DNA-binding, helix-turn-helix (HTH) domain of about 65 amino acids. It is present in transcription regulators of the LuxR/FixJ family of response regulators. The domain is named after Vibrio fischeri luxR, a transcriptional activator for quorum-sensing control of luminescence. LuxR-type HTH domain proteins occur in a variety of organisms. The DNA-binding HTH domain is usually located in the C-terminal region of the protein; the N-terminal region often containing an autoinducer-binding domain or a response regulatory domain. Most luxR-type regulators act as transcription activators, but some can be repressors or have a dual role for different sites. LuxR-type HTH regulators control a wide variety of activities in various biological processes.

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Acyl-homoserine-lactone synthase is an enzyme with systematic name acyl-(acyl-carrier protein):S-adenosyl-L-methionine acyltranserase . This enzyme catalyses the following chemical reaction

Acyl-homoserine lactone acylase may refer to:

Acyl-homoserine-lactone acylase (EC 3.5.1.97, acyl-homoserine lactone acylase, AHL-acylase, AiiD, N-acyl-homoserine lactone acylase, PA2385 protein, quorum-quenching AHL acylase, quorum-quenching enzyme, PvdQ, QuiP) is an enzyme with systematic name N-acyl-L-homoserine-lactone amidohydrolase. This enzyme functions as a quorum quencher by catalysing the following chemical reaction

Variovorax paradoxus is a gram negative, beta proteobacterium from the genus Variovorax. Strains of V. paradoxus can be categorized into two groups, hydrogen oxidizers and heterotrophic strains, both of which are aerobic. The genus name Vario-vorax and species name para-doxus (contrary-opinion) reflects both the dichotomy of V. paradoxus metabolisms, but also its ability to utilize a wide array of organic compounds.

<i>Myxococcus</i> Genus of bacteria

Myxococcus is a genus of bacteria in the family Myxococcaceae. Myxococci are Gram-negative, spore-forming, chemoorganotrophic, obligate aerobes. They are elongated rods with rounded or tapered ends, and they are nonflagellated. The cells move by gliding and can predate other bacteria. The genus has been isolated from soil.

Diffusible signal factor (DSF) is found in several gram-negative bacteria and play a role in the formation of biofilms, motility, virulence, and antibiotic resistance. Xanthomonas campestris was the first bacteria known to have DSF. The synthesis of the DSF can be seen in rpfF and rpfB enzymes. An understanding of the DSF signaling mechanism could lead to further disease control.

References

  1. ↑ Fuqua, C.; Winans, S. C.; Greenberg, E. P. (1996). "Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum-sensing transcriptional regulators". Annu. Rev. Microbiol. 50: 727–751. doi:10.1146/annurev.micro.50.1.727. PMID   8905097.
  2. ↑ Thomas PW, Stone EM, Costello AL, Tierney DL, Fast W (May 2005). "The quorum-quenching lactonase from Bacillus thuringiensis is a metalloprotein". Biochemistry. 44 (20): 7559–69. doi:10.1021/bi050050m. PMID   15895999.
  3. ↑ Dong YH, Gusti AR, Zhang Q, Xu JL, Zhang LH (April 2002). "Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species". Applied and Environmental Microbiology. 68 (4): 1754–9. doi:10.1128/AEM.68.4.1754-1759.2002. PMC   123891 . PMID   11916693.
  4. ↑ Wang LH, Weng LX, Dong YH, Zhang LH (April 2004). "Specificity and enzyme kinetics of the quorum-quenching N-Acyl homoserine lactone lactonase (AHL-lactonase)". The Journal of Biological Chemistry. 279 (14): 13645–51. doi: 10.1074/jbc.M311194200 . PMID   14734559.
  5. ↑ Dong YH, Xu JL, Li XZ, Zhang LH (March 2000). "AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora". Proceedings of the National Academy of Sciences of the United States of America. 97 (7): 3526–31. doi: 10.1073/pnas.060023897 . PMC   16273 . PMID   10716724.
  6. ↑ Dong YH, Wang LH, Xu JL, Zhang HB, Zhang XF, Zhang LH (June 2001). "Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase". Nature. 411 (6839): 813–7. doi:10.1038/35081101. PMID   11459062. S2CID   4324448.
  7. ↑ Lee SJ, Park SY, Lee JJ, Yum DY, Koo BT, Lee JK (August 2002). "Genes encoding the N-acyl homoserine lactone-degrading enzyme are widespread in many subspecies of Bacillus thuringiensis". Applied and Environmental Microbiology. 68 (8): 3919–24. doi:10.1128/aem.68.8.3919-3924.2002. PMC   124016 . PMID   12147491.
  8. ↑ Park SY, Lee SJ, Oh TK, Oh JW, Koo BT, Yum DY, Lee JK (June 2003). "AhlD, an N-acylhomoserine lactonase in Arthrobacter sp., and predicted homologues in other bacteria". Microbiology. 149 (Pt 6): 1541–50. doi: 10.1099/mic.0.26269-0 . PMID   12777494.
  9. ↑ Ulrich RL (October 2004). "Quorum quenching: enzymatic disruption of N-acylhomoserine lactone-mediated bacterial communication in Burkholderia thailandensis". Applied and Environmental Microbiology. 70 (10): 6173–80. doi:10.1128/AEM.70.10.6173-6180.2004. PMC   522112 . PMID   15466564.
  10. ↑ Kim MH, Choi WC, Kang HO, Lee JS, Kang BS, Kim KJ, Derewenda ZS, Oh TK, Lee CH, Lee JK (December 2005). "The molecular structure and catalytic mechanism of a quorum-quenching N-acyl-L-homoserine lactone hydrolase". Proceedings of the National Academy of Sciences of the United States of America. 102 (49): 17606–11. doi: 10.1073/pnas.0504996102 . PMC   1295591 . PMID   16314577.
  11. ↑ Liu D, Lepore BW, Petsko GA, Thomas PW, Stone EM, Fast W, Ringe D (August 2005). "Three-dimensional structure of the quorum-quenching N-acyl homoserine lactone hydrolase from Bacillus thuringiensis". Proceedings of the National Academy of Sciences of the United States of America. 102 (33): 11882–7. doi: 10.1073/pnas.0505255102 . PMC   1187999 . PMID   16087890.
  12. ↑ Yang F, Wang LH, Wang J, Dong YH, Hu JY, Zhang LH (July 2005). "Quorum quenching enzyme activity is widely conserved in the sera of mammalian species". FEBS Letters. 579 (17): 3713–7. doi: 10.1016/j.febslet.2005.05.060 . PMID   15963993.
  13. ↑ Dong, Y.; Wang, L.; Xu, J.; Zhang, H.; Zhang, X.; Zhang, L. (2001). "Quencing quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase". Nature. 411 (6839): 813–817. Bibcode:2001Natur.411..813D. doi:10.1038/35081101. PMID   11459062. S2CID   4324448.
  14. ↑ Thomas P. W.; Stone E. M.; Costello A. L.; Tierney D. L.; Fast W. (2005). "The quorum-quenching lactonase from Bacillus thuringiensis is a metalloprotein". Biochemistry. 44 (20): 7559–7569. doi:10.1021/bi050050m. PMID   15895999.
  15. ↑ Momb J.; Wang C.; Liu D.; Thomas P. W.; Petsko G. A.; Guo H.; Ringe D; Fast W. (2008). "Mechanism of the quorum-quenching lactonae (AiiA) from Bacillus thuringiensis. 2. Substrate modeling and active site mutations". Biochemistry. 47 (29): 7715–7725. doi:10.1021/bi8003704. PMC   2646874 . PMID   18627130.
  16. ↑ Riaz K.; Elmerich, C.; Moreira, D.; Raffoux A.; Dessaux Y.; Faure D. (2008). "A metagenomic analysis of soil bacteria extends the diversity of quorum-quenching lactonases". Environmental Microbiology. 10 (3): 560–570. doi:10.1111/j.1462-2920.2007.01475.x. PMID   18201196.
  17. ↑ Schipper C.; Hornung C.; Bijtenhoorn P.; Quitschau M.; Grond S.; Streit W. R. (2009). "Metagenome-derived clones encoding two novel lactonase family proteins involved in biofilm inhibition in Pseudomonas aeruginosa". Applied and Environmental Microbiology. 75 (1): 224–233. doi:10.1128/aem.01389-08. PMC   2612230 . PMID   18997026.
  18. 1 2 Dong Y. H.; Gusti A. R.; Zhang Q.; Xu J. L.; Zhang, L. H. (2002). "Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species". Applied and Environmental Microbiology. 68 (4): 1754–1759. doi:10.1128/AEM.68.4.1754-1759.2002. PMC   123891 . PMID   11916693.
  19. ↑ Haudecoeur E.; Tannieres M.; Cirou A.; Raffoux A; Dessaux Y.; Faure D. (2009). "Different regulation and roles of lactonases AiiB and AttM in Agrobacterium tumefaciens C58". Molecular Plant-Microbe Interactions. 22 (5): 529–537. doi:10.1094/MPMI-22-5-0529. PMID   19348571.
  20. 1 2 Chistiakov DA, Melnichenko AA, Orekhov AN, Bobryshev YV (2017). "Paraoxonase and atherosclerosis-related cardiovascular diseases". Biochimie . 132: 19–27. doi:10.1016/j.biochi.2016.10.010. PMID   27771368.
  21. ↑ Leadbetter, J. R. G.; Greenberg, E. P. (2000). "Metabolism of acyl-homoserine lactone quorum-sensing signals by Variovorax paradoxus". J. Bacteriol. 182 (24): 6921–6926. doi:10.1128/JB.182.24.6921-6926.2000. PMC   94816 . PMID   11092851.
  22. ↑ Rasmussen T. B.; Givskov M. (2006). "Quorum-sensing inhibitors as anti-pathogenic drugs". International Journal of Medical Microbiology . 296 (2–3): 149–161. doi:10.1016/j.ijmm.2006.02.005. PMID   16503194.
  23. ↑ Whitehead, N. A.; Barnard A. M. L.; Slater H.; Simpson, N. J. L.; Salmond, G. P. C. (2001). "Quorum sensing in Gram-negative bacteria". FEMS Microbiol. Rev. 25 (4): 365–404. doi: 10.1111/j.1574-6976.2001.tb00583.x . PMID   11524130..
  24. ↑ Smith R. S.; Iglewski B. H. (2003). "P. aeruginosa quorum-sensing systems and virulence". Current Opinion in Microbiology. 6 (1): 56–60. doi:10.1016/S1369-5274(03)00008-0. PMID   12615220.
  25. ↑ Pirhonen, M.; Flegom, D.; Heikinheimo, R.; Palva, E. T. (1993). "A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora". EMBO J. 12 (6): 2467–2476. doi:10.1002/j.1460-2075.1993.tb05901.x. PMC   413482 . PMID   8508772.
  26. ↑ Von Bodman S. B.; Bauer W. D.; Coplin D. L. (2003). "Quorum-sensing in plant-pathogenic bacteria". Annual Review of Phytopathology. 41: 455–482. doi:10.1146/annurev.phyto.41.052002.095652. PMID   12730390.
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