Oceanic Hitchhikers – Assessing Pathogen Risks from Marine Microplastic

Abstract

Microplastics are a major source of anthropogenic contamination in the oceans. This contamination is now widespread, recalcitrant, and likely to continue unabated into the future.Plastics represent an important environmental substrate for the colonisation of bacteria from the surrounding water column, with distinct communities, abundances, and population structures on the plastic surfaces.There is the potential for microplastics to act as a long-distance transport mechanism for human and animal pathogens, potentially spreading pathogenic bacteria into new areas.A variety of human pathogens have been found on microplastics in the open ocean, but we do not know their pathogenicity and virulence potential or what, if any, human pathogen transmission occurs via this route.There is increasing scientific consensus that microplastics may act as vectors for the spread of antimicrobial-resistance genes. As plastic debris in the environment continues to increase, an emerging concern is the potential for microplastic to act as vectors for pathogen transport. With aquaculture the fastest growing food sector, and microplastic contamination of shellfish increasingly demonstrated, understanding any risk of pathogen transport associated with microplastic is important for this industry. However, there remains a lack of detailed, systematic studies assessing the interactions and potential impacts that the attachment of human and animal pathogens on microplastic may have. Here we synthesise current knowledge regarding these distinct microplastic-associated bacterial communities and microplastic uptake pathways into bivalves, and discuss whether they represent a human and animal health threat, highlighting the outstanding questions critical to our understanding of this potential risk to food safety. As plastic debris in the environment continues to increase, an emerging concern is the potential for microplastic to act as vectors for pathogen transport. With aquaculture the fastest growing food sector, and microplastic contamination of shellfish increasingly demonstrated, understanding any risk of pathogen transport associated with microplastic is important for this industry. However, there remains a lack of detailed, systematic studies assessing the interactions and potential impacts that the attachment of human and animal pathogens on microplastic may have. Here we synthesise current knowledge regarding these distinct microplastic-associated bacterial communities and microplastic uptake pathways into bivalves, and discuss whether they represent a human and animal health threat, highlighting the outstanding questions critical to our understanding of this potential risk to food safety. Plastic pollution is now ubiquitous within marine environments globally [1.Isobe A. et al.Abundance of non-conservative microplastics in the upper ocean from 1957 to 2066.Nat. Commun. 2019; 10: 1-3Crossref PubMed Scopus (205) Google Scholar], with an estimated 15–51 trillion plastic particles floating on the surface of the world’s oceans [2.van Sebille E. et al.A global inventory of small floating plastic debris.Environ. Res. Lett. 2015; 10: 1-11Crossref Scopus (936) Google Scholar]. This likely represents only ~1% of the 4.8–12.7 million tons of the plastics thought to enter global oceans annually [3.Jambeck J. et al.Plastic waste inputs from land into ocean.Mar. Pollut. 2015; 347: 3-6Google Scholar], with a significant input known to come via rivers, and the majority of microplastic eventually sinking via fouling, flocculation, and egestion processes [4.Porter A. et al.Role of marine snows in microplastic fate and bioavailability.Environ. Sci. Technol. 2018; 52: 7111-7119Crossref PubMed Scopus (205) Google Scholar]. Microplastic is now considered to be a global concern due to its widespread presence within aquatic and terrestrial food webs, including many commercially important species used for human consumption, encompassing zooplankton, bivalves, crustaceans, fish and other marine vertebrates [5.Peng L. et al.Micro- and nano-plastics in marine environment: Source, distribution and threats — A review.Sci. Total Environ. 2020; 698: 134254Crossref PubMed Scopus (314) Google Scholar]. Whilst a range of impacts of macroplastic (see Glossary) and microplastic upon organism health, and some effects on the ecosystem, have been reported (e.g., [6.Bucci K. et al.What is known and unknown about the effects of plastic pollution: A meta-analysis and systematic review.Ecol. Appl. 2020; 30: 1-16Crossref Scopus (244) Google Scholar]), an emerging threat which, until recently, has received less attention is the potential for plastic debris to act as novel substrates for pathogens, in particular marine bacteria such as vibrios (e.g., [7.Zettler E.R. et al.Life in the 'plastisphere': Microbial communities on plastic marine debris.Environ. Sci. Technol. 2013; 47: 7137-7146Crossref PubMed Scopus (1500) Google Scholar,8.Amaral-Zettler L.A. et al.Ecology of the plastisphere.Nat. Rev. Microbiol. 2020; 18: 139-151Crossref PubMed Scopus (429) Google Scholar]), and as carriers of antimicrobial-resistant bacteria. This is of particular concern for food safety given the growing body of evidence of microplastic uptake by commercial seafood and aquaculture shellfish species. Here, we synthesise the current understanding and discuss the critical knowledge gaps regarding the potential threat of transport of pathogens via microplastic and its risk to aquaculture species and food security. The surface properties of plastic are thought to play an important part in determining its ecological impacts [9.Galloway T.S. et al.Interactions of microplastic debris throughout the marine ecosystem.Nat. Ecol. Evol. 2017; 1: 1-8Crossref PubMed Scopus (898) Google Scholar]. The smooth, hydrophobic surfaces of virgin (unfouled) plastics have no net charge, but this rapidly changes once in seawater as organic matter, biomolecules, nutrients, and bacteria, as well as hazardous hydrophobic contaminants, quickly sorb to the polymer surface. This sorption of biological materials produces a unique ecocorona [9.Galloway T.S. et al.Interactions of microplastic debris throughout the marine ecosystem.Nat. Ecol. Evol. 2017; 1: 1-8Crossref PubMed Scopus (898) Google Scholar] which, as demonstrated by ecotoxicology studies, can influence both biological uptake of nanoparticles and their fate within tissues and cells (e.g., [10.Nasser F. Lynch I. Secreted protein eco-corona mediates uptake and impacts of polystyrene nanoparticles on Daphnia magna.J. Proteome. 2016; 137: 45-51Crossref PubMed Scopus (212) Google Scholar]). The selective binding of secretory molecules, including infochemicals or protein signalling molecules, to microplastic may also influence their ecological interactions within marine ecosystems. For example, dimethyl sulfide (DMS) – an infochemical, released during zooplankton grazing on phytoplankton, which stimulates feeding activity in a range of planktivorous species (e.g., [11.Nevitt G.A. et al.Foraging cue for Antarctic procellariiform seabirds.Nature. 1995; 376: 680-682Crossref Scopus (270) Google Scholar]) – can be produced by the fouling communities present on microplastic [12.Savoca M.S. et al.Marine plastic debris emits a keystone infochemical for olfactory foraging seabirds.Sci. Adv. 2016; 2: 1-9Crossref Scopus (161) Google Scholar]; this then increases the frequency of plastic ingestion by copepods [13.Procter J. et al.Smells good enough to eat: Dimethyl sulfide (DMS) enhances copepod ingestion of microplastics.Mar. Pollut. Bull. 2019; 138: 1-6Crossref PubMed Scopus (55) Google Scholar] and seabirds [12.Savoca M.S. et al.Marine plastic debris emits a keystone infochemical for olfactory foraging seabirds.Sci. Adv. 2016; 2: 1-9Crossref Scopus (161) Google Scholar]. Hence microplastic can take on a chemical profile that might mask its polymer properties and even act to facilitate accidental ingestion and uptake into tissues. The attachment of harmful microbes to plastic debris was first observed by Masó et al. [14.Masó M. et al.Drifting plastic debris as a potential vector for dispersing Harmful Algal Bloom (HAB) species.Sci. Mar. 2003; 67: 107-111Crossref Scopus (222) Google Scholar]. However, it was the landmark paper by Zettler et al. [7.Zettler E.R. et al.Life in the 'plastisphere': Microbial communities on plastic marine debris.Environ. Sci. Technol. 2013; 47: 7137-7146Crossref PubMed Scopus (1500) Google Scholar], first describing the ‘plastisphere’, that highlighted the potential for marine microplastics to house distinct communities of microbes on their surfaces. It has since been widely demonstrated that, in seawater, plastic surfaces will quickly develop a conditioning film, and subsequently, a biofilm taxonomically distinct to that of the surrounding seawater [7.Zettler E.R. et al.Life in the 'plastisphere': Microbial communities on plastic marine debris.Environ. Sci. Technol. 2013; 47: 7137-7146Crossref PubMed Scopus (1500) Google Scholar,15.Oberbeckmann S. et al.Environmental factors support the formation of specific bacterial assemblages on microplastics.Front. Microbiol. 2018; 8: 2709Crossref PubMed Scopus (263) Google Scholar]. Of particular concern are the increasing reports of the presence of numerous pathogenic microbes on both macro- and microplastic surfaces from across oceanic regions. Vibrios, in particular, have been found in high abundances within plastisphere communities, particularly in the summer months [7.Zettler E.R. et al.Life in the 'plastisphere': Microbial communities on plastic marine debris.Environ. Sci. Technol. 2013; 47: 7137-7146Crossref PubMed Scopus (1500) Google Scholar,8.Amaral-Zettler L.A. et al.Ecology of the plastisphere.Nat. Rev. Microbiol. 2020; 18: 139-151Crossref PubMed Scopus (429) Google Scholar,16.Frère L. et al.Microplastic bacterial communities in the Bay of Brest: Influence of polymer type and size.Environ. Pollut. 2018; PubMed Scopus Google et of microplastics with of bacteria on the surface of microplastics in Environ. 2020; PubMed Scopus Google et of microplastics on bacterial biofilm formation and their potential threat to A in on the Pollut. 2020; PubMed Scopus Google Scholar] in L. et al.Microplastic bacterial communities in the Bay of Brest: Influence of polymer type and size.Environ. Pollut. 2018; PubMed Scopus Google et of microplastics with of bacteria on the surface of microplastics in Environ. 2020; PubMed Scopus Google et of microplastics on bacterial biofilm formation and their potential threat to A in on the Pollut. 2020; PubMed Scopus Google et bacterial of microplastics in Microbiol. PubMed Scopus Google et of potentially pathogenic bacteria by plastic debris in Pollut. Bull. 2019; PubMed Scopus Google et of bacteria on organic particles and surrounding Pollut. 2018; PubMed Scopus Google S. et on a and influence of microbes marine plastic 2016; Scopus Google et for potentially pathogenic on microplastic Environ. Res. 2016; 1-8Crossref PubMed Scopus Google et as a vector for the transport of the bacterial fish pathogen species Pollut. Bull. 2017; PubMed Scopus Google A. et of plastic by E. Pollut. Bull. 2019; PubMed Scopus Google et al.Marine microplastic-associated bacterial in to and plastic type in Pollut. Bull. 2019; PubMed Scopus Google K. et environmental biofilm assemblages on microplastics in Microbiol. 2019; 10: PubMed Google et of bacterial communities on plastic debris by environmental factors and polymer in the of Sci. Technol. 2019; PubMed Scopus Google E. of bacterial assemblages from microplastics of Total Environ. 2019; PubMed Scopus Google Scholar]). – not of which are pathogenic – are in the open ocean, high of vibrios have been reported on microplastic from the [7.Zettler E.R. et al.Life in the 'plastisphere': Microbial communities on plastic marine debris.Environ. Sci. Technol. 2013; 47: 7137-7146Crossref PubMed Scopus (1500) Google Scholar,8.Amaral-Zettler L.A. et al.Ecology of the plastisphere.Nat. Rev. Microbiol. 2020; 18: 139-151Crossref PubMed Scopus (429) Google Scholar]. with the long-distance potential of floating microplastic et potential of marine species long-distance Ecol. 2019; Scopus Google Scholar], the important as to whether the increasing of plastic waste in global oceans for vibrios and other pathogens to be and to potential to of to the by including are known to be associated with a variety of substrates such as and even et of Rev. PubMed Scopus Google S. et transmission of pathogenic species by a potential threat to the 2019; PubMed Scopus Google S. M. assemblages on and in Rev. Mar. Sci. 2020; PubMed Scopus Google Scholar], which act to the of vibrios and a of transport across oceanic environments et of Rev. PubMed Scopus Google Scholar]. The of pathogenic microbes on particles of to may be meta-analysis that the abundances of a variety of potentially pathogenic species found on microplastic across the the and the with present on particles within the S. M. assemblages on and in Rev. Mar. Sci. 2020; PubMed Scopus Google Scholar]. to whether microplastic to the risk of pathogen and other by of floating there are a of factors to in 1: the attachment processes and interactions (e.g., of on the the and of transport of particles across and whether the plastisphere changes as plastics transport processes to the ingestion and the uptake and of particles into and the of as a and of which might influence the risk to human on of the the of on and in and The is on pathogens that to of the for the they et for potentially pathogenic on microplastic Environ. Res. 2016; 1-8Crossref PubMed Scopus Google et as a vector for the transport of the bacterial fish pathogen species Pollut. Bull. 2017; PubMed Scopus Google Bay of L. et al.Microplastic bacterial communities in the Bay of Brest: Influence of polymer type and size.Environ. Pollut. 2018; PubMed Scopus Google and A. et of plastic by E. Pollut. Bull. 2019; PubMed Scopus Google bacterial was not in this paper – the of plastic that by or et of microplastics with of bacteria on the surface of microplastics in Environ. 2020; PubMed Scopus Google et al.Marine microplastic-associated bacterial in to and plastic type in Pollut. Bull. 2019; PubMed Scopus Google K. et environmental biofilm assemblages on microplastics in Microbiol. 2019; 10: PubMed Google et of bacterial communities on plastic debris by environmental factors and polymer in the of Sci. Technol. 2019; PubMed Scopus Google E. of bacterial assemblages from microplastics of Total Environ. 2019; PubMed Scopus Google et bacterial of microplastics in Microbiol. PubMed Scopus Google and et of potentially pathogenic bacteria by plastic debris in Pollut. Bull. 2019; PubMed Scopus Google and et of microplastics on bacterial biofilm formation and their potential threat to A in on the Pollut. 2020; PubMed Scopus Google and et of bacteria on organic particles and surrounding Pollut. 2018; PubMed Scopus Google S. et on a and influence of microbes marine plastic 2016; Scopus Google The bacterial was not in this paper – the of plastic that by or in a new are of or species of to a surface and in an et interactions in bacterial interactions in Rev. Microbiol. PubMed Scopus Google Scholar]. The unique and that rapidly on microplastic surfaces likely play a in the unique plastisphere communities that on in K. et the of the aquatic plastic pollution and Lett. 2017; 2: Scopus Google J. The chemical of microplastics in marine environment: A Pollut. Bull. 2019; PubMed Scopus Google Scholar]). The of this biofilm formation are the environmental of the surrounding seawater, with polymer type thought to play a less significant L.A. et al.Ecology of the plastisphere.Nat. Rev. Microbiol. 2020; 18: 139-151Crossref PubMed Scopus (429) Google Scholar,15.Oberbeckmann S. et al.Environmental factors support the formation of specific bacterial assemblages on microplastics.Front. Microbiol. 2018; 8: 2709Crossref PubMed Scopus (263) Google K. et environmental biofilm assemblages on microplastics in Microbiol. 2019; 10: PubMed Google et of bacterial communities on plastic debris by environmental factors and polymer in the of Sci. Technol. 2019; PubMed Scopus Google Scholar]. within a biofilm is and can microbes to as reported for with of and et of on a as for aquatic Ecol. Scopus Google Scholar]. vibrios rapidly associated with to in However, whether a biofilm is for pathogenic species to be present within the and biofilm formation processes might from on remains is thought to within microplastic microbes M. et al.Microplastic pollution increases in aquatic Pollut. 2018; PubMed Scopus Google Scholar] and can to the formation of pathogenicity for and S. et and of pathogenicity and in environmental 2018; 8: PubMed Scopus Google Scholar]. bacteria have been reported on microplastic surfaces in the surrounding seawater et of microplastics with of bacteria on the surface of microplastics in Environ. 2020; PubMed Scopus Google et in the marine environment are for and 2019; PubMed Scopus Google Scholar]. organic can also and in some pathogenic microbes is found in seawater et of on a as for aquatic Ecol. Scopus Google Scholar]. However, in with seawater and the plastisphere has significant in the pathways that to et of microplastics on bacterial biofilm formation and their potential threat to A in on the Pollut. 2020; PubMed Scopus Google Scholar]. microplastic may not act only as a for pathogens, it may also pathogenic which have and other properties is as a critical global and there is increasing that the environment a in the and of the there has been increasing concern that microplastic represents an important environmental for the and spread of et al. et in the marine environment are for and 2019; PubMed Scopus Google Scholar] the and of and and their within the from plastic particles in the found that the of both and in the on plastics was it was in seawater et in the marine environment are for and 2019; PubMed Scopus Google Scholar]. studies have also that microplastic a in both the of communities and the of including frequency of in bacteria associated with microplastic – with bacteria or in – has been observed and to in the spread of M. et al.Microplastic pollution increases in aquatic Pollut. 2018; PubMed Scopus Google Scholar], the this are microplastics can as vectors for harmful – in with other microbes and including which for – microplastics act as a for bacteria. particular, bacterial communities present in are spreading and of J. PubMed Scopus Google Scholar] such as both the of and the and of on microplastic particles are and of plastics are for transport via surface et of floating debris in the world’s Pollut. Bull. PubMed Scopus Google Scholar]. are a major source of microplastics and pathogenic microbes in et of water by pathogenic 1-16Crossref PubMed Scopus Google J. et global of microplastics to the marine environment: and Total Environ. 2019; PubMed Scopus Google Scholar]. A of microplastic particles from and it has been reported that the plastisphere communities that are to these particles from the in the surrounding environment of the the plastisphere has also been reported to pathogenic species et of microplastic and bacterial assemblages in surface and of an Sci. 2017; Scopus Google Scholar] – the of the of the world’s in pathogenic plastic debris has been to the transport of species across oceanic (e.g., S. et on on of in the Pollut. Bull. 2018; 137: PubMed Scopus Google Scholar]) it is to the plastisphere is as particles across do plastisphere communities and to the environment as they are oceanic evidence that the is by the and environmental of the seawater the microplastic to the that plastisphere communities will and to as they are oceanic this has been in a S. M. assemblages on and in Rev. Mar. Sci. 2020; PubMed Scopus Google et of microplastic and bacterial assemblages in surface and of an Sci. 2017; Scopus Google Scholar]. This for the chemical to a microplastic surface in with the surrounding seawater et al.Microplastic as a vector for in the aquatic environment: critical and of Sci. Technol. 2016; PubMed Scopus Google Scholar]. processes are not well for plastisphere communities, and there are increasing reports of potential pathogens microplastic in with if any, of the potential pathogen However, studies to that have pathogenic species have the only and not the this not for the of the plastisphere as a et of potentially pathogenic bacteria by plastic debris in Pollut. Bull. 2019; PubMed Scopus Google et for potentially pathogenic on microplastic Environ. Res. 2016; 1-8Crossref PubMed Scopus Google Scholar]. this of that the attachment of pathogenic microbes to microplastic systematic such as (e.g., and a of ecological – of the surrounding water et aquaculture in and of Scopus Google Scholar] and of This is to microplastic with a of both and studies that and take microplastic particles from their surrounding seawater et in and water the emerging of global Mar. 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The of to microplastic is to since microplastic will and be likely to the and of the on a of the microplastic of the the of the of of and a growing global human aquaculture is to be the only to seafood that global marine are reported and Commun. 2016; PubMed Scopus Google Scholar]. The and has the for a of by to global with a million within the The of and Scholar]. is now the fastest growing food sector, in of seafood for human M. et aquaculture to the global food Sci. S. A. PubMed Scopus Google Scholar], with many for in the and et of marine and pathways 2019; Scopus Google Scholar]. The of the to of is of the by the aquaculture et marine and aquaculture Rev. Mar. 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Microplastic has been in commercial bivalves, including and global microplastic aquaculture a of of high aquaculture in microplastic pathogen such as microplastic particles in the commercially important have been reported J. et in commercial from Pollut. 2015; PubMed Scopus Google Scholar]. the also has high microplastic abundances, in this the of microplastic particles is highlighting the of microplastic pollution [2.van Sebille E. et al.A global inventory of small floating plastic debris.Environ. Res. Lett. 2015; 10: 1-11Crossref Scopus (936) Google Scholar]. The global distribution of microplastic may to be considered in the of aquaculture if pathogen is demonstrated to be a to this threat is the knowledge as to whether ingestion of microplastic can to if the studies have now that pathogen from plastic to may [7.Zettler E.R. et al.Life in the 'plastisphere': Microbial communities on plastic marine debris.Environ. Sci. Technol. 2013; 47: 7137-7146Crossref PubMed Scopus (1500) Google Scholar,16.Frère L. et al.Microplastic bacterial communities in the Bay of Brest: Influence of polymer type and size.Environ. Pollut. 2018; PubMed Scopus Google et for potentially pathogenic on microplastic Environ. Res. 2016; 1-8Crossref PubMed Scopus Google Scholar] but have not demonstrated this plastic debris is associated with for in the the of within increases from to associated with plastic debris et al.Plastic waste associated with on 2018; PubMed Scopus Google Scholar]. the to pathogen via microplastic of from the surface of microplastic to the tissues of the was demonstrated protein E. microplastic ingestion et and of microplastic ingestion by the Sci. 2019; PubMed Scopus Google Scholar]. This that pathogen from to can evidence the of microplastic as a pathogen this occurs in other marine such as bivalves, and its to and human health is unknown and is a for questions regarding the of bacteria and microplastic in the open ocean (see in may now to these bacteria and their interactions with microplastic particles across environmental to these the in in the has been the in and A bacterial can now be within and then and in less have produced of our current knowledge describing the bacterial of plastisphere communities in in are and are to these and interactions on these surfaces. of the is – which can quickly and et bacterial from 2020; PubMed Scopus Google Scholar]. these are also there is now potential to these in of to be within and in such as and will also to microplastic particles to the of bacteria in both and such will to and bacteria present on microplastic and potentially their abundances, as well as and virulence genes. a there is growing evidence to that microplastic represent a potential of pathogens and on these distinct that from particles Whilst attachment of and other pathogens to microplastic is well the effects that this may for any potential to aquaculture are to be the factors bacterial attachment to microplastic are also unknown and The potential that this may to the aquaculture sector, as well as the for human health, are and is in to a into this increasing This is an of that will marine and is the fate and transport of pathogens across oceans and into marine species by microplastics if to that by the bacterial communities on microplastics represent only the they are for example, environments or are communities by microplastic is by microplastic it a concern for human marine also to to are these animal and human and and are these pathogen from microplastic to organism if this the of can we human health from microplastics in the marine environment and within aquaculture is the fate and transport of pathogens across oceans and into marine species by microplastics if to that by the bacterial communities on microplastics represent only the they are for example, environments or are communities by microplastic is by microplastic it a concern for human marine also to to are these animal and human and and are these pathogen from microplastic to organism if this the of can we human health from microplastics in the marine environment and within aquaculture is by we for their support of this and are by to for with the with of for the for the microplastic abundances of commercial species in associated within the ecological the of a body of the of microbes via via the of a surface of organic such as and that are known to and any surface in an aquatic a chemical that and as a of by to or of plastic the to in of marine a from studies that the of plastic the is to in some the range is and a of that that pathogenicity or virulence to a a on the surface of a plastic in this the of plastic particles that have been by a species to its by a that and a pathogen from to

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