Microbial Ecotoxicology of Marine Plastic Debris: A Review on Colonization and Biodegradation by the "Plastisphere"

Abstract

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.

Keywords: bacteria; biodegradation; colonization; marine plastics debris; metabolic pathways.

FIGURE 1

Illustration of the potential impact of plastic in the regulatory role of carbon and nutrient cycles played by bacteria via the microbial loop. Dissolve (DOM) and particulate (POM) organic matter originated from the linear trophic chain is returned to higher trophic levels via its incorporation in bacterial biomass.

FIGURE 2

The different steps of plastic biodegradation at sea (modified from Dussud and Ghiglione, 2014).

FIGURE 3

Current standards on biodegradability of plastics at sea. ISO 18830: Plastics-determination of aerobic biodegradation of non-floating plastic materials in a seawater/ sandy sediment interface – Method by measuring the oxygen demand in closed respirometer. ISO 19679: Determination of aerobic biodegradation of non-floating plastic materials in a seawater/sediment interface – method by analysis of evolved carbon dioxide respirometer. ASTMD7991: Determining aerobic biodegradation of plastics buried in sandy marine sediment under controlled laboratory conditions. ASTM D7473: Standard test method for weight attrition of plastic materials in the marine environment by open system aquarium incubations. ASTM: Standard test method for determining aerobic biodegradation of plastic materials in the marine environment by a defined microbial consortium or natural sea water inoculum.

FIGURE 4

Biodegradation pathways under aerobic conditions of three conventional plastics (polyethylene, polyethylene terephthalate, and polystyrene) and one biodegradable plastic (polyhydroxybutyrate). See explanation in the text indicating that degradation rates may be very different between polymer types. Complete mineralisation into CO₂ and H₂O occurred after several steps of transformation of the initial molecule involving several microbial enzymes. The common stage of transformation through the TCA cycle produce also ATP, which is a key component for bacterial growth and biomass production. Enzyme commission numbers (EC numbers) were given for each enzyme-catalyzed reactions. EC 3.1.1.76, poly(3-hydroxyoctanoate) depolymerase; EC 2.3.1.16, acetyl-CoA C-acyltransferase; EC 1.1.1.35, 3-hydroxyacyl-CoA dehydrogenase; EC 1.3.8.7, medium-chain acyl-CoA dehydrogenase; EC 4.2.1.17, enoyl-CoA hydratase; EC 3.1.1.101, poly(ethylene terephthalate) hydrolase; EC 3.1.1.102, Mono(2-hydroxyethyl) terephthalate hydrolase; EC 1.14.12.15, terephthalate 1,2-dioxygenase; EC 1.3.1.53, 3,4-dihydroxycyclohexa-1,5-diene-1,4-dicarboxylate dehydrogenase; EC 1.13.11.8, protocatechuate 4,5-dioxygenase; EC 1, Oxidoreductase; EC 3, Hydrolase; EC 1.14.14, 11 styrene monooxygenase; EC 5.3.99.7, styrene-oxide isomerase; EC 1.2.1.39, phenylacetaldehyde dehydrogenase; EC 6.2.1.30, phenylacetylCoA ligase; EC 1.14.13.149, phenylacetyl-CoA 1,2-epoxidase; EC 1.14.13, ring 1,2-epoxyphenylacetyl-CoA isomerase; EC 1.2.1.91, 3-oxo-5,6-dehydrosuberyl-CoA semialdehyde dehydrogenase; EC 2.3.1.174, 3-oxoadipyl-CoA/3-oxo-5,6-dehydrosuberyl-CoA thiolase; EC 4.2.1.17, 2,3-dehydroadipyl-CoA hydratase; EC 1.1.1.35, 3-hydroxyadipyl-CoA dehydrogenase.