Diversity and Activity of Communities Inhabiting Plastic Debris in the North Pacific Gyre

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 oceanograph...

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Autores principales: Jessica A. Bryant, Tara M. Clemente, Donn A. Viviani, Allison A. Fong, Kimberley A. Thomas, Paul Kemp, David M. Karl, Angelicque E. White, Edward F. DeLong
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Publicado: American Society for Microbiology 2016
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spelling oai:doaj.org-article:6b415c3f9ed442be95d43d858c25fc792021-12-02T19:47:34ZDiversity and Activity of Communities Inhabiting Plastic Debris in the North Pacific Gyre10.1128/mSystems.00024-162379-5077https://doaj.org/article/6b415c3f9ed442be95d43d858c25fc792016-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00024-16https://doaj.org/toc/2379-5077ABSTRACT 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 5 mm and >5 mm) 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.Jessica A. BryantTara M. ClementeDonn A. VivianiAllison A. FongKimberley A. ThomasPaul KempDavid M. KarlAngelicque E. WhiteEdward F. DeLongAmerican Society for MicrobiologyarticleNorth Pacific Gyrebiofilmsmicrobial communitiesmicroplasticsMicrobiologyQR1-502ENmSystems, Vol 1, Iss 3 (2016)
institution DOAJ
collection DOAJ
language EN
topic North Pacific Gyre
biofilms
microbial communities
microplastics
Microbiology
QR1-502
spellingShingle North Pacific Gyre
biofilms
microbial communities
microplastics
Microbiology
QR1-502
Jessica A. Bryant
Tara M. Clemente
Donn A. Viviani
Allison A. Fong
Kimberley A. Thomas
Paul Kemp
David M. Karl
Angelicque E. White
Edward F. DeLong
Diversity and Activity of Communities Inhabiting Plastic Debris in the North Pacific Gyre
description 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 5 mm and >5 mm) 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.
format article
author Jessica A. Bryant
Tara M. Clemente
Donn A. Viviani
Allison A. Fong
Kimberley A. Thomas
Paul Kemp
David M. Karl
Angelicque E. White
Edward F. DeLong
author_facet Jessica A. Bryant
Tara M. Clemente
Donn A. Viviani
Allison A. Fong
Kimberley A. Thomas
Paul Kemp
David M. Karl
Angelicque E. White
Edward F. DeLong
author_sort Jessica A. Bryant
title Diversity and Activity of Communities Inhabiting Plastic Debris in the North Pacific Gyre
title_short Diversity and Activity of Communities Inhabiting Plastic Debris in the North Pacific Gyre
title_full Diversity and Activity of Communities Inhabiting Plastic Debris in the North Pacific Gyre
title_fullStr Diversity and Activity of Communities Inhabiting Plastic Debris in the North Pacific Gyre
title_full_unstemmed Diversity and Activity of Communities Inhabiting Plastic Debris in the North Pacific Gyre
title_sort diversity and activity of communities inhabiting plastic debris in the north pacific gyre
publisher American Society for Microbiology
publishDate 2016
url https://doaj.org/article/6b415c3f9ed442be95d43d858c25fc79
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