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Enzymatic Potential of Alcanivorax to Degrade Natural and Synthetic Polyesters

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Enzymatic Potential of Alcanivorax to Degrade Natural and Synthetic Polyesters Environmental Microbiology (2020) 22(4), 1356–1369 doi:10.1111/1462-2920.14947 Beyond oil degradation: enzymatic potential of Alcanivorax to degrade natural and synthetic polyesters Vinko Zadjelovic,1* Audam Chhun,1 enormous potential for biodegrading aliphatic poly- Mussa Quareshy,1 Eleonora Silvano,1 esters thanks to a unique and abundantly secreted Juan R. Hernandez-Fernaud,1,2 alpha/beta hydrolase. The heterologous over- María M. Aguilo-Ferretjans,1,3 Rafael Bosch,3,4 expression of this esterase proved a remarkable abil- Cristina Dorador,5,6,7 Matthew I. Gibson8,9 and ity to hydrolyse both natural and synthetic Joseph A. Christie-Oleza 1,3,4* polyesters. Our findings contribute to (i) better under- 1School of Life Sciences, University of Warwick, stand the ecology of Alcanivorax in its natural envi- Warwick, UK. ronment, where natural polyesters such as 2Unidad de investigación-HUC, La Laguna-Tenerife, polyhydroxyalkanoates (PHA) are produced by a Spain. large fraction of the community and, hence, an acces- 3Department of Biology, University of the Balearic sible source of carbon and energy used by the organ- Islands, Spain. ism in order to persist, (ii) highlight the potential of Alcanivorax 4IMEDEA (CSIC-UIB), Esporles, Spain. to clear marine environments from poly- 5Laboratorio de Complejidad Microbiana y Ecología ester materials of anthropogenic origin as well as Funcional, Universidad de Antofagasta, Antofagasta, oils, and (iii) the discovery of a new versatile esterase Chile. with a high biotechnological potential. 6Departamento de Biotecnología, Universidad de Antofagasta, Antofagasta, Chile. Introduction 7 Centre for Biotechnology & Bioengineering (CeBiB), In microbial ecology, the idea that ‘everything is every- Santiago, Chile. where, but, the environment selects’ (Baas-Becking, 8 Department of Chemistry, University of Warwick, 1934; De Wit and Bouvier, 2006) requires that even the Warwick, UK. rare biota has to persist through time via the assimilation 9 Warwick Medical School, University of Warwick, of a source of carbon and energy, unless they are able to Warwick, UK. remain dormant such as by sporulation. Marine ecosys- tems are mostly oligotrophic and hostile to non-adapted Summary microorganisms due to the lack of nutrients and high salinity. The predominant heterotrophic bacteria that Pristine marine environments are highly oligotrophic inhabit these environments are thus well adapted to such ecosystems populated by well-established special- conditions and have mainly specialized in the use of ized microbial communities. Nevertheless, during oil labile substrates released by marine phototrophs spills, low-abundant hydrocarbonoclastic bacteria (Sharma et al., 2014; Christie-Oleza et al., 2017; bloom and rapidly prevail over the marine microbiota. Bakenhus et al., 2018; Zheng et al., 2019). The genus Alcanivorax is one of the most abundant Alcanivorax is a ubiquitous marine bacterial genus and well-studied organisms for oil degradation. While classed as an obligate hydrocarbonoclastic bacterium highly successful under polluted conditions due to (OHCB) due to its preference to metabolize hydrocarbons its specialized oil-degrading metabolism, it is and crude oil derivatives (Yakimov et al., 2019). This unknown how they persist in these environments during pristine conditions. Here, we show that part of genus rapidly blooms and becomes one of the most the Alcanivorax genus, as well as oils, has an abundant organisms during marine pollution events and oil-spills (Kasai et al., 2002; Hara et al., 2003); however, how does Alcanivorax persist within the rare biome of Received 16 December, 2019; accepted 18 February, 2020. *For pristine seawater while awaiting favourable conditions? correspondence. E-mail [email protected]; Tel: (+00) 34 – 971172738; Fax: (+00) 34 971173184. E-mail v.zadjelovic@warwick. Although members of the Alcanivorax genus can grow ac.uk although inefficiently – with more labile substrates such © 2020 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Polyesters degradation by Alcanivorax 1357 as pyruvate and succinate (Fernández-Martínez et al., Hence, although some marine microbial isolates have 2003; Naether et al., 2013; Radwan et al., 2019), they been reported to degrade a range of polyesters (Mabrouk would be outcompeted by other heterotrophic bacteria in and Sabry, 2001; Ghanem et al., 2005; Sekiguchi et al., the natural environment (McGenity et al., 2012; Yakimov 2010), such a process is not as obvious in marine envi- et al., 2019). It has been suggested, although, that ronments as highlighted by studies that failed to observe Alcanivorax spp. may persist in pristine environments by degradation of some theoretically biodegradable poly- using alkanes released by marine cyanobacteria (Coates mers such as PHB, PES and PBS (Sekiguchi et al., et al., 2014; Lea-Smith et al., 2015) and other 2010; Bagheri et al., 2017). hydrocarbon-producing eukaryotic algae (Sorigué et al., In this study, we characterize a novel and versatile 2016, 2017). The hydrolysis of aliphatic polyesters such esterase secreted by Alcanivorax that hydrolyses a num- as poly(caprolactone) (PCL), poly(hydroxybutylate) ber of natural and synthetic polyesters, that is, PHB, (PHB) and poly(butylene succinate) (PBS) by some PHBV, PES, PBS and PCL. Altogether, the evidence Alcanivorax isolates has also been shown (Sekiguchi here suggests that the environmental relevance of the et al., 2011; Zadjelovic et al., 2019), although the underly- genus Alcanivorax goes beyond the degradation of solely ing molecular mechanisms behind the ability of these oil-derived compounds. strains to degrade such polyesters remained unknown. Interestingly, during the screening for polylactic acid (PLA) esterases, researchers identified that the enzyme Results ABO2449 encoded by Alcanivorax borkumensis had a Polyester degradation by Alcanivorax sp. 24 strong hydrolytic activity on PLA as well as on a range of other aliphatic polyesters, that is, poly(hydroxybutylate- Alcanivorax sp. 24, isolated from marine plastic debris co-valerate) (PHBV), PCL and poly(ethylene succinate) (Zadjelovic et al., 2019), produced clear degradation (PES) (Hajighasemi et al., 2016). halos on plates containing the polyesters PHB, PHBV, A large number of environmental microbes – including PES, PBS and PCL (Fig. 1A and Table 1). Although the members from the genus Alcanivorax – synthesize intra- degradation of the natural polymers PHB and PHBV was cellular aliphatic polyester granules, that is, polyhydroxy expected because the strain was originally enriched and alkanoates (PHA), as a strategy to store carbon and isolated on PHB (Zadjelovic et al., 2019), the large degra- energy when nutrient availability is imbalanced (e.g. dation halos on the synthetic polyesters PES, PBS and under high C:N conditions; Fernández-Martínez et al., PCL within just 3–6 days was remarkable and deserved 2003; Sabirova et al., 2006; Jendrossek and Pfeiffer, further investigation. Growth curves of Alcanivorax sp. 24 2014). As well as aliphatic polyesters of natural origin (e. were conducted with polyesters PHB, PHBV and PES to g. the PHAs: PHB and PHBV), in recent years, there has assess if the bacterium could assimilate and grow on been an increase of industrially manufactured synthetic these polymers as well as degrade them (Fig. 1B). Pro- polyesters (e.g. PLA, PCL, PES or PBS; Flieger et al., tein quantification was used as a proxy for growth 2003; Tseng et al., 2007). Aliphatic polyesters are tagged because standard monitoring techniques (e.g. turbidity or as ‘biodegradable plastics,’ and although they still repre- colony forming units) could not be performed due to poly- sent a small fraction of the global polymer material mar- mer insolubility. Interestingly, Alcanivorax sp. 24 was ket, the consumer demand of these environmentally able to grow on all polymers faster than with the labile friendly alternatives to traditional non-biodegradable control substrate, that is, succinate, particularly with PHB materials is exponentially growing (Tokiwa et al., 2009; (i.e. ~150 μg of protein/ml at day four; Fig. 1B). Aeschelmann and Carus, 2015). Like all plastics, ali- We also assayed if Alcanivorax sp. 24 could degrade phatic polyesters also find their way into the oceans bis[2-hydroxyethyl] terephthalate (BHET; Table 1), an (Jambeck et al., 2015; Lebreton et al., 2017). Although intermediate of the recalcitrant polyester polyethylene considered biodegradable because their linking ester terephthalate (PET). When grown on BHET, Alcanivorax bonds are susceptible to hydrolysis by esterases, lipases sp. 24 produced apparent clumpy growth in liquid cul- or other enzymes (Nakajima-Kambe et al., 1999; Müller tures and it decreased the white turbidity of this insoluble et al., 2001; Zheng et al., 2005; Shah et al., 2014), other compound (Fig. 1C). Unfortunately, BHET interfered with factors such as chemical structure, molecular weight, the protein quantification method producing a large back- hydrophobicity and crystallinity may hinder degradability ground signal, and hence, growth quantification was not of these materials (Tokiwa et al., 2009). Furthermore, possible. To overcome the difficulties in measuring bacte- polymer degradation in marine
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