Over the last decades, it has become clear that plastic pollution presents a global societal and environmental challenge given its increasing presence in the oceans. A growing literature has focused on the microbial life growing on the surfaces of these pollutants called the “plastisphere,” but the general concepts of microbial ecotoxicology have only rarely been integrated. Microbial ecotoxicology deals with (i) the impact of pollutants on microbial communities and inversely (ii) how much microbes can influence their biodegradation. The goal of this review is to enlighten the growing literature of the last 15 years on microbial ecotoxicology related to plastic pollution in the oceans. First, we focus on the impact of plastic on marine microbial life and on the various functions it ensures in the ecosystems. In this part, we also discuss the driving factors influencing biofilm development on plastic surfaces and the potential role of plastic debris as vector for dispersal of harmful pathogen species. Second, we give a critical view of the extent to which marine microorganisms can participate in the decomposition of plastic in the oceans and of the relevance of current standard tests for plastic biodegradability at sea. We highlight some examples of metabolic pathways of polymer biodegradation. We conclude with several questions regarding gaps in current knowledge of plastic biodegradation by marine microorganisms and the identification of possible directions for future research.
Plastics are ubiquitous in the oceans and constitute suitable matrices for bacterial attachment and growth. Understanding biofouling mechanisms is a key issue to assessing the ecological impacts and fate of plastics in marine environment. In this study, we investigated the different steps of plastic colonization of polyolefin-based plastics, on the first one hand, including conventional low-density polyethylene (PE), additivated PE with pro-oxidant (OXO), and artificially aged OXO (AA-OXO); and of a polyester, poly(3-hydroxybutyrate-co-3-hydroxyvalerate) (PHBV), on the other hand. We combined measurements of physical surface properties of polymers (hydrophobicity and roughness) with microbiological characterization of the biofilm (cell counts, taxonomic composition, and heterotrophic activity) using a wide range of techniques, with some of them used for the first time on plastics. Our experimental setup using aquariums with natural circulating seawater during 6 weeks allowed us to characterize the successive phases of primo-colonization, growing, and maturation of the biofilms. We highlighted different trends between polymer types with distinct surface properties and composition, the biodegradable AA-OXO and PHBV presenting higher colonization by active and specific bacteria compared to non-biodegradable polymers (PE and OXO). Succession of bacterial population occurred during the three colonization phases, with hydrocarbonoclastic bacteria being highly abundant on all plastic types. This study brings original data that provide new insights on the colonization of non-biodegradable and biodegradable polymers by marine microorganisms.
The thin film of life that inhabits all plastics in the oceans, so-called “plastisphere,” has multiple effects on the fate and impacts of plastic in the marine environment. Here, we aimed to evaluate the relative influence of the plastic size, shape, chemical composition, and environmental changes such as a phytoplankton bloom in shaping the plastisphere abundance, diversity and activity. Polyethylene (PE) and polylactide acid (PLA) together with glass controls in the forms of meso-debris (18 mm diameter) and large-microplastics (LMP; 3 mm diameter), as well as small-microplastics (SMP) of 100 μm diameter with spherical or irregular shapes were immerged in seawater during 2 months. Results of bacterial abundance (confocal microscopy) and diversity (16S rRNA Illumina sequencing) indicated that the three classical biofilm colonization phases (primo-colonization after 3 days; growing phase after 10 days; maturation phase after 30 days) were not influenced by the size and the shape of the materials, even when a diatom bloom (Pseudo-nitzschia sp.) occurred after the first month of incubation. However, plastic size and shape had an effect on bacterial activity (3H leucine incorporation). Bacterial communities associated with the material of 100 μm size fraction showed the highest activity compared to all other material sizes. A mature biofilm developed within 30 days on all material types, with higher bacterial abundance on the plastics compared to glass, and distinct bacterial assemblages were detected on each material type. The diatom bloom event had a great impact on the plastisphere of all materials, resulting in a drastic change in diversity and activity. Our results showed that the plastic size and shape had relatively low influence on the plastisphere abundance, diversity, and activity, as compared to the plastic composition or the presence of a phytoplankton bloom.
The European Parliament recently approved a new law banning single-use plastic items for 2021 such as plastic plates, cutlery, straws, cotton swabs, and balloon sticks. Transition to a bioeconomy involves the substitution of these banned products with biodegradable materials. Several materials such as polylactic acid (PLA), polybutylene adipate terephthalate (PBAT), poly(butylene succinate) (PBS), polyhydroxybutyrate-valerate (PHBV), Bioplast, and Mater-Bi could be good candidates to substitute cotton swabs, but their biodegradability needs to be tested under marine conditions. In this study, we described the microbial life growing on these materials, and we evaluated their biodegradability in seawater, compared with controls made of non-biodegradable polypropylene (PP) or biodegradable cellulose. During the first 40 days in seawater, we detected clear changes in bacterial diversity (Illumina sequencing of 16S rRNA gene) and heterotrophic activity (incorporation of 3H-leucine) that coincided with the classic succession of initial colonization, growth, and maturation phases of a biofilm. Biodegradability of the cotton swab sticks was then tested during another 94 days under strict diet conditions with the different plastics as sole carbon source. The drastic decrease of the bacterial activity on PP, PLA, and PBS suggested no bacterial attack of these materials, whereas the bacterial activity in PBAT, Bioplast, Mater-Bi, and PHBV presented similar responses to the cellulose positive control. Interestingly, the different bacterial diversity trends observed for biodegradable vs. non-biodegradable plastics allowed to describe potential new candidates involved in the degradation of these materials under marine conditions. This better understanding of the bacterial 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.
Many bacteria, such as Proteobacteria, Cyanobacteria and Bacteroidetes, use N-acylhomoserine lactones (AHLs) as quorum-sensing (QS) signal molecules for communication. Enzymatic degradation of AHLs, such as AHL acylase and AHL lactonase, can degrade AHLs (quorum quenching, QQ) to attenuate or disarm the virulence of pathogens. QQ is confirmed to be common in marine bacterial communities. Many genes encoding AHL acylases are found in marine bacteria and metagenomic collections, but only a few of these have been characterized in detail. We have reported that the marine bacterium Pseudoalteromonas flavipulchra JG1 can degrade AHLs. In the present study, a novel AHL acylase PfmA, which can degrade AHLs with acyl chains longer than 10 carbons, was identified from strain JG1. Ultra-performance liquid chromatography (UPLC) and electrospray ionization mass spectrometry (ESI-MS) analysis demonstrated that PfmA functions as an AHL acylase, which hydrolysed the amide bond of AHL. The purified PfmA of P. flavipulchra JG1 showed optimum activity at 30 °C and pH 7.0. PfmA belongs to the N-terminal nucleophile (Ntn) hydrolase superfamily and showed homology to a member of penicillin amidases, but PfmA can degrade ampicillin but not penicillin G. The residue Ser256 in PfmA is the active site according to site-directed mutagenesis. Furthermore, PfmA reduced AHL accumulation and the production of virulence factors in Vibrio anguillarum VIB72 and Pseudomonas aeruginosa PAO1, and attenuated the virulence of P. aeruginosa to increase Artemia survival, which suggested that PfmA can be considered as a therapeutic agent to control AHL-mediated pathogenicity.
Halomonas bacteria are ubiquitous in global marine environments, however, their sulfur-oxidizing abilities and survival adaptations in hydrothermal environments are not well understood. In this study, we characterized the sulfur oxidation ability and metabolic mechanisms of Halomonas titanicae SOB56, which was isolated from the sediment of the Tangyin hydrothermal field in the Southern Okinawa Trough. Physiological characterizations showed that it is a heterotrophic sulfur-oxidizing bacterium that can oxidize thiosulfate to tetrathionate, with the Na2S2O3 degradation reaching 94.86%. Two potential thiosulfate dehydrogenase-related genes, tsdA and tsdB, were identified as encoding key catalytic enzymes, and their expression levels in strain SOB56 were significantly upregulated. Nine of fifteen examined Halomonas genomes possess TsdA- and TsdB-homologous proteins, whose amino acid sequences have two typical Cys-X2-Cys-His heme-binding regions. Moreover, the thiosulfate oxidation process in H. titanicae SOB56 might be regulated by quorum sensing, and autoinducer-2 synthesis protein LuxS was identified in its genome. Regarding the mechanisms underlying adaptation to hydrothermal environment, strain SOB56 was capable of forming biofilms and producing EPS. In addition, genes related to complete flagellum assembly system, various signal transduction histidine kinases, heavy metal transporters, anaerobic respiration, and variable osmotic stress regulation were also identified. Our results shed light on the potential functions of heterotrophic Halomonas bacteria in hydrothermal sulfur cycle and revealed possible adaptations for living at deep-sea hydrothermal fields by H. titanicae SOB56.
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