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Microbial Diversity and Activity During the Biodegradation in Seawater of Various Substitutes to Conventional Plastic Cotton Swab Sticks

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Microbial Diversity and Activity During the Biodegradation in Seawater of Various Substitutes to Conventional Plastic Cotton Swab Sticks fmicb-12-604395 July 15, 2021 Time: 14:48 # 1 ORIGINAL RESEARCH published: 15 July 2021 doi: 10.3389/fmicb.2021.604395 Microbial Diversity and Activity During the Biodegradation in Seawater of Various Substitutes to Conventional Plastic Cotton Swab Sticks Justine Jacquin1,2, Nolwenn Callac1,3, Jingguang Cheng1, Carolane Giraud1,3, Yonko Gorand4, Clement Denoual5, Mireille Pujo-Pay1, Pascal Conan1, Anne-Leila Meistertzheim6, Valerie Barbe7, Stéphane Bruzaud5 and Jean-François Ghiglione1* 1 CNRS, UMR 7621, Laboratoire d’Océanographie Microbienne, Observatoire Océanologique de Banyuls, Sorbonne Edited by: Université, Paris, France, 2 Innovation Plasturgie et Composites, Biopole Clermont Limagne, Saint-Beauzire, France, 3 CNRS, Mechthild Schmitt-Jansen, UMR 9220 ENTROPIE, Ifremer (LEAD-NC), IRD, Univ Nouvelle–Calédonie, Univ La Réunion, Nouméa, New Caledonia, Helmholtz Centre for Environmental 4 Plateforme EnRMAT, Laboratoire PROMES, Rembla de la Thermodynamique, Perpignan, France, 5 UMR CNRS 6027, Research (UFZ), Germany Institut de Recherche Dupuy de Lôme (IRDL), Université de Bretagne-Sud, Lorient, France, 6 SAS Plastic@Sea, Observatoire Océanologique de Banyuls, Banyuls-sur-Mer, France, 7 Génomique Métabolique, Genoscope, Institut François Jacob, CEA, Reviewed by: CNRS, Univ Evry, Université Paris-Saclay, Evry, France Gabriela Vázquez-Rodríguez, Autonomous University of the State of Hidalgo, Mexico The European Parliament recently approved a new law banning single-use plastic items Christian Lott, HYDRA Marine Sciences GmbH, for 2021 such as plastic plates, cutlery, straws, cotton swabs, and balloon sticks. Germany Transition to a bioeconomy involves the substitution of these banned products with *Correspondence: biodegradable materials. Several materials such as polylactic acid (PLA), polybutylene Jean-François Ghiglione adipate terephthalate (PBAT), poly(butylene succinate) (PBS), polyhydroxybutyrate- [email protected] valerate (PHBV), Bioplast, and Mater-Bi could be good candidates to substitute cotton Specialty section: swabs, but their biodegradability needs to be tested under marine conditions. In this This article was submitted to study, we described the microbial life growing on these materials, and we evaluated Microbiotechnology, a section of the journal their biodegradability in seawater, compared with controls made of non-biodegradable Frontiers in Microbiology polypropylene (PP) or biodegradable cellulose. During the first 40 days in seawater, Received: 09 September 2020 we detected clear changes in bacterial diversity (Illumina sequencing of 16S rRNA Accepted: 12 May 2021 3 Published: 15 July 2021 gene) and heterotrophic activity (incorporation of H-leucine) that coincided with the Citation: classic succession of initial colonization, growth, and maturation phases of a biofilm. Jacquin J, Callac N, Cheng J, Biodegradability of the cotton swab sticks was then tested during another 94 days Giraud C, Gorand Y, Denoual C, under strict diet conditions with the different plastics as sole carbon source. The Pujo-Pay M, Conan P, Meistertzheim A-L, Barbe V, drastic decrease of the bacterial activity on PP, PLA, and PBS suggested no bacterial Bruzaud S and Ghiglione J-F (2021) attack of these materials, whereas the bacterial activity in PBAT, Bioplast, Mater-Bi, and Microbial Diversity and Activity During the Biodegradation in Seawater PHBV presented similar responses to the cellulose positive control. Interestingly, the of Various Substitutes to Conventional different bacterial diversity trends observed for biodegradable vs. non-biodegradable Plastic Cotton Swab Sticks. plastics allowed to describe potential new candidates involved in the degradation of Front. Microbiol. 12:604395. doi: 10.3389/fmicb.2021.604395 these materials under marine conditions. This better understanding of the bacterial Frontiers in Microbiology| www.frontiersin.org 1 July 2021| Volume 12| Article 604395 fmicb-12-604395 July 15, 2021 Time: 14:48 # 2 Jacquin et al. Marine Plastisphere Activity and Diversity diversity and activity dynamics during the colonization and biodegradation processes contributes to an expanding baseline to understand plastic biodegradation in marine conditions and provide a foundation for further decisions on the replacement of the banned single-used plastics. Keywords: plastisphere, biofouling, plastic biodegradation, single-used plastics, microbial colonization INTRODUCTION microorganisms colonizing plastics in natural conditions, also known as the “plastisphere” (Zettler et al., 2013) which is still The growing worldwide use of plastics together with waste poorly studied. In addition, the conventional techniques used mismanagement resulted in an estimated release of more than to measure the biodegradation activity by evolution of O2 or five trillion plastic particles weighing over 250,000 tons afloat CO2 generally require substantial equipment and can limit the in the oceans, resulting in dramatic toxicological effects along number of experimental replicates. Other activity tests can be the marine trophic chain (Eriksen et al., 2014; Wang et al., considered as alternative methods, such as the use of radiolabeled 2019). A large majority of plastic items found at sea is made leucine incorporation that has been used for decades in marine of polyethylene (PE), polypropylene (PP), and polystyrene (PS), microbiology (Kirchman et al., 1985) or tests based on ATP which are more likely to float, and polyvinyl chloride (PVC), measurements (Fontanella et al., 2013). When introduced in nylons, and polyethylene terephthalate (PET), which are more seawater, plastics are rapidly colonized by bacteria. This process likely to sink (Auta et al., 2017). has been extensively studied, showing successive phases of Government regulations have been recently established biofilm formation (Dang and Lovell, 2000; Lobelle and Cunliffe, to restrict the use of single-use plastics and promote the 2011; Eich et al., 2015; Erni-Cassola et al., 2019). During the first biodegradable plastic industry. For example, since 2018, at least days at sea, a “conditioning film” made of inorganic and organic 127 countries have established regulations against plastic bags matter supports the initial colonization phase generally initiated (UNEP, 2018). The European Parliament voted to ban many by Gammaproteobacteria and Alphaproteobacteria, regardless other single-use plastics for 2021, including plates, cutlery, straws, of the material type (Oberbeckmann et al., 2015). A second food containers, and expanded polystyrene cups as well as phase of rapidly growing bacteria is then usually characterized sticks used for cotton swabs and plastic balloons (Europarl, by a succession of Bacteroidetes, Acidobacteria, Actinobacteria, 2019). Biodegradable plastics have become the focus of recent Cyanobacteria, Firmicutes, and Planctomycetes (Salta et al., researches in order to replace conventional materials made of 2013). The last phase corresponds to a mature biofilm that PE, PP, PS, PVC, PET, and other high-molecular compounds. generally appears after 15–30 days at sea and remains stable Today, commercially available biodegradable materials are of for several months, and where clear differences in bacterial petrochemical origin, such as poly(butylene succinate) (PBS) abundance, diversity and activity, were found between non- and polybutylene adipate terephthalate (PBAT; brand name biodegradable and biodegradable plastics (Eich et al., 2015; Ecoflex R ), or are bio-based such as polylactic acid (PLA) and Dussud et al., 2018). Hydrocarbonoclastic bacteria (HCB) such as polyhydroxybutyrate-valerate (PHBV). Natural starch is also Alcanivorax sp., Aestuariicella hydrocarbonica, and Marinobacter frequently offered as a solution, blended with petrochemical- sp. became abundant in the mature biofilm and were suggested to based (mainly potato starch for Bioplast©) or bio-based materials be potentially involved in the degradation of fossil-based plastics. (corn starch with PBAT for Mater-Bi©). However, no study has extended the experience by incubating the Plastic biodegradation is the microbial conversion of all its mature biofilm in minimum medium with the plastic as the only organic constituents to carbon dioxide, new microbial biomass carbon source in order to prove its biodegradation capabilities. and mineral salts under oxic conditions, or to carbon dioxide, Here, we used hollow cylinder sticks, such as those used methane, new microbial biomass, and mineral salts, under anoxic for cotton swabs, made of different conventional (PP) and conditions (Science Advice for Policy by European Academies “biodegradable” materials as potential candidates for substitutes [SAPEA], 2020). The biodegradability of a plastic is defined to conventional single-use plastics (PLA, PBS, PBAT, Mater- according to several standards reflecting disposal condition in Bi, Bioplast, PHBV, and cellulose). We hypothesized that the soil, compost, or aquatic environments. Tests are generally properties of the distinct materials would select different marine based on respirometry (biological oxygen demand and CO2 bacterial communities with specific biodegradation capabilities. production) attributed to the biodegradation of the plastic by We elaborated an original two-step experimental design based microbial communities, without any other source of carbon in on a first colonization step in natural seawater (40 days) followed artificial medium, in comparison with cellulose, which serves as by a second step of incubation in minimum
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