Annonaceous acetogenins as biofilm formation promoters: Challenges in increasing the efficiency of PAHs biodegradation processes.

Abstract

Polycyclic aromatic hydrocarbons (PAHs) are present in the environment and producedby many human activities; therefore, they are easily found in air, water and soil. Manyorganizations have listed them as priority pollutants that should be eliminated becauseof their carcinogenic and toxic effects; thus, their microbial degradation has becomecrucial. Naphthalene serves as a model for understanding the properties of a wide rangeof environmentally relevant PAHs.Biofilms are microbial communities that allow bioremediation processes to be moreefficient and durable. This subject is widely discussed in the literature and, among otherissues, is supported by the fact that biofilm cells are protected within a matrix.Enhancing the formation of bacterial biofilms by means of natural products likeannonaceous acetogenins might be considered as a interesting strategy forbioremediation.In our laboratory, many experiments were carried out to decrease the rates of PAHsemploying biofilm forming bacteria as bioremediators. Among several strains isolatedfrom intertidal sediments of the southern coasts of Argentina, Pseudomonasplecoglossicida J26 was the best naphthalene degrading microorganism.Annonaceous acetogenins (ACG) are secondary metabolites that display a wide range ofbiological activities like a potent cytotoxicity that implies interaction at membranelevel, and the selective inhibition of the mitochondrial complex I. ACG, particularlysquamocin and laherradurin, have the ability, even at very low concentrations (2.5μg/ml), to stimulate biofilm formation of PAHs degrading strains like Pseudomonasplecoglossicida J26.Biofilm formation is often regulated by a cell density-dependent signalling systemcalled quorum sensing (QS). We have determined that P. plecoglossicida J26 regulatesits biofilm production by N-acylhomoserine lactone (AHL) mediated QS mechanism.The ACG laherradurin and squamocin are indirectly involved in quorum sensingmechanism by inducing a stress related increase in AHL production which in turnstimulates biofilm formation without detriment on bacterial growth.In order to establish a relationship between naphthalene degradation and biofilmformation capacities of P. plecoglossicida J26 in presence of ACG, PAHs and biofilmwere quantified simultaneously. The addition of ACG in batch planktonic cultures withdeveloping biofilm stimulated biofilm formation and the rate of naphthaleneconsumption was substantially increased. The degradation abilities of P. plecoglossicidaJ26 biofilm, in the absence of planktonic cells, produced higher quantities of biofilm inpresence of ACG, leading to an increased rate of naphthalene degradation.Laboratory scale batch reactor results open new perpectives in the search of differentACG and their derivatives for being more efficient in the degradation of PAHs mediatedby P. plecoglossicida J26.In conclusion, ACG or supernatants from cell cultures grown in their presence, can actas biofilm formation promoters that could increase the efficiency of bioremediationprocesses.