Abstract
Marine plastic debris has become a significant concern in ocean ecosystems worldwide. Little is known, however, about its influence on microbial community structure and function. In 2008, we surveyed microbial communities and metabolic activities in seawater and on plastic on an oceanographic expedition through the "great Pacific garbage patch." The concentration of plastic particles in surface seawater within different size classes (2 to 5mm and >5mm) ranged from 0.35 to 3.7 particles m-3 across sampling stations. These densities and the particle size distribution were consistent with previous values reported in the North Pacific Ocean. Net community oxygen production (NCP = gross primary production - community respiration) on plastic debris was positive and so net autotrophic, whereas NCP in bulk seawater was close to zero. Scanning electron microscopy and metagenomic sequencing of plastic-attached communities revealed the dominance of a few metazoan taxa and a diverse assemblage of photoautotrophic and heterotrophic protists and bacteria. Bryozoa, Cyanobacteria, Alphaproteobacteria, and Bacteroidetes dominated all plastic particles, regardless of particle size. Bacteria inhabiting plastic were taxonomically distinct from the surrounding picoplankton and appeared well adapted to a surface-associated lifestyle. Genes with significantly higher abundances among plastic-attached bacteria included che genes, secretion system genes, and nifH genes, suggesting enrichment for chemotaxis, frequent cell-to-cell interactions, and nitrogen fixation. In aggregate, our findings suggest that plastic debris forms a habitat for complex microbial assemblages that have lifestyles, metabolic pathways, and biogeochemical activities that are distinct from those of free-living planktonic microbial communities. IMPORTANCE Marine plastic debris is a growing concern that has captured the general public's attention. While the negative impacts of plastic debris on oceanic macrobiota, including mammals and birds, are well documented, little is known about its influence on smaller marine residents, including microbes that have key roles in ocean biogeochemistry. Our work provides a new perspective on microbial communities inhabiting microplastics that includes its effect on microbial biogeochemical activities and a description of the cross-domain communities inhabiting plastic particles. This study is among the first molecular ecology, plastic debris biota surveys in the North Pacific Subtropical Gyre. It has identified fundamental differences in the functional potential and taxonomic composition of plastic-associated microbes versus planktonic microbes found in the surrounding open-ocean habitat. Author Video: An author video summary of this article is available.
Highlights
Marine plastic debris has become a significant concern in ocean ecosystems worldwide
Our work provides a new perspective on microbial communities inhabiting microplastics that includes its effect on microbial biogeochemical activities and a description of the cross-domain communities inhabiting plastic particles
The distribution of plastic particle sizes was reasonably modeled with a power law scaling exponent in the size bins above 3 mm, but below which plastic concentrations begin to decrease (Fig. 2)
Summary
Marine plastic debris has become a significant concern in ocean ecosystems worldwide. This study is among the first molecular ecology, plastic debris biota surveys in the North Pacific Subtropical Gyre It has identified fundamental differences in the functional potential and taxonomic composition of plastic-associated microbes versus planktonic microbes found in the surrounding open-ocean habitat. In 1988, scientists correctly predicted that buoyant plastic debris entering the ocean would become concentrated in regions termed “gyres,” where large-scale subtropical currents converge [5]. This prediction has since been confirmed by multiple sampling efforts spanning the Pacific and Atlantic Ocean Gyres [3, 6,7,8,9]. Small plastic particles, including those called microplastics (generally Ͻ5 mm in size, but see reference 24), may be harmful, given that they are more abundant and that their reduced size makes them ingestible by small grazers that form the lower levels of the marine trophic system [24]
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