Identification of rare microbial colonizers of plastic materials incubated in a coral reef environment

Plastic waste accumulation in marine environments has complex, unintended impacts on ecology that cross levels of community organization. To measure succession in polyolefin-colonizing marine bacterial communities, an in situ time-series experiment was conducted in the oligotrophic coastal waters of...

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Main Authors: Sebastian L. Singleton, Edward W. Davis, Holly K. Arnold, An Mei Y. Daniels, Susanne M. Brander, Rachel J. Parsons, Thomas J. Sharpton, Stephen J. Giovannoni
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-10-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1259014/full
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author Sebastian L. Singleton
Edward W. Davis
Holly K. Arnold
An Mei Y. Daniels
Susanne M. Brander
Rachel J. Parsons
Thomas J. Sharpton
Stephen J. Giovannoni
author_facet Sebastian L. Singleton
Edward W. Davis
Holly K. Arnold
An Mei Y. Daniels
Susanne M. Brander
Rachel J. Parsons
Thomas J. Sharpton
Stephen J. Giovannoni
author_sort Sebastian L. Singleton
collection DOAJ
description Plastic waste accumulation in marine environments has complex, unintended impacts on ecology that cross levels of community organization. To measure succession in polyolefin-colonizing marine bacterial communities, an in situ time-series experiment was conducted in the oligotrophic coastal waters of the Bermuda Platform. Our goals were to identify polyolefin colonizing taxa and isolate bacterial cultures for future studies of the biochemistry of microbe-plastic interactions. HDPE, LDPE, PP, and glass coupons were incubated in surface seawater for 11 weeks and sampled at two-week intervals. 16S rDNA sequencing and ATR-FTIR/HIM were used to assess biofilm community structure and chemical changes in polymer surfaces. The dominant colonizing taxa were previously reported cosmopolitan colonizers of surfaces in marine environments, which were highly similar among the different plastic types. However, significant differences in rare community composition were observed between plastic types, potentially indicating specific interactions based on surface chemistry. Unexpectedly, a major transition in community composition occurred in all material treatments between days 42 and 56 (p < 0.01). Before the transition, Alteromonadaceae, Marinomonadaceae, Saccharospirillaceae, Vibrionaceae, Thalassospiraceae, and Flavobacteriaceae were the dominant colonizers. Following the transition, the relative abundance of these taxa declined, while Hyphomonadaceae, Rhodobacteraceae and Saprospiraceae increased. Over the course of the incubation, 8,641 colonizing taxa were observed, of which 25 were significantly enriched on specific polyolefins. Seven enriched taxa from families known to include hydrocarbon degraders (Hyphomonadaceae, Parvularculaceae and Rhodobacteraceae) and one n-alkane degrader (Ketobacter sp.). The ASVs that exhibited associations with specific polyolefins are targets of ongoing investigations aimed at retrieving plastic-degrading microbes in culture.
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spelling doaj.art-de87d42fa6bc477dba3095e816f228a72023-10-05T11:43:19ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-10-011410.3389/fmicb.2023.12590141259014Identification of rare microbial colonizers of plastic materials incubated in a coral reef environmentSebastian L. Singleton0Edward W. Davis1Holly K. Arnold2An Mei Y. Daniels3Susanne M. Brander4Rachel J. Parsons5Thomas J. Sharpton6Stephen J. Giovannoni7Department of Microbiology, Oregon State University, Corvallis, OR, United StatesDepartment of Microbiology, Oregon State University, Corvallis, OR, United StatesDepartment of Microbiology, Oregon State University, Corvallis, OR, United StatesBermuda Institute of Ocean Sciences, St. George's, BermudaDepartment of Fisheries, Wildlife, and Conservation Sciences, Coastal Oregon Marine Experiment Station, Oregon State University, Newport, OR, United StatesBermuda Institute of Ocean Sciences, St. George's, BermudaDepartment of Microbiology, Oregon State University, Corvallis, OR, United StatesDepartment of Microbiology, Oregon State University, Corvallis, OR, United StatesPlastic waste accumulation in marine environments has complex, unintended impacts on ecology that cross levels of community organization. To measure succession in polyolefin-colonizing marine bacterial communities, an in situ time-series experiment was conducted in the oligotrophic coastal waters of the Bermuda Platform. Our goals were to identify polyolefin colonizing taxa and isolate bacterial cultures for future studies of the biochemistry of microbe-plastic interactions. HDPE, LDPE, PP, and glass coupons were incubated in surface seawater for 11 weeks and sampled at two-week intervals. 16S rDNA sequencing and ATR-FTIR/HIM were used to assess biofilm community structure and chemical changes in polymer surfaces. The dominant colonizing taxa were previously reported cosmopolitan colonizers of surfaces in marine environments, which were highly similar among the different plastic types. However, significant differences in rare community composition were observed between plastic types, potentially indicating specific interactions based on surface chemistry. Unexpectedly, a major transition in community composition occurred in all material treatments between days 42 and 56 (p < 0.01). Before the transition, Alteromonadaceae, Marinomonadaceae, Saccharospirillaceae, Vibrionaceae, Thalassospiraceae, and Flavobacteriaceae were the dominant colonizers. Following the transition, the relative abundance of these taxa declined, while Hyphomonadaceae, Rhodobacteraceae and Saprospiraceae increased. Over the course of the incubation, 8,641 colonizing taxa were observed, of which 25 were significantly enriched on specific polyolefins. Seven enriched taxa from families known to include hydrocarbon degraders (Hyphomonadaceae, Parvularculaceae and Rhodobacteraceae) and one n-alkane degrader (Ketobacter sp.). The ASVs that exhibited associations with specific polyolefins are targets of ongoing investigations aimed at retrieving plastic-degrading microbes in culture.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1259014/fullplastispheremicrobiomepolyolefinsmicrobial successionin situ16S rDNA
spellingShingle Sebastian L. Singleton
Edward W. Davis
Holly K. Arnold
An Mei Y. Daniels
Susanne M. Brander
Rachel J. Parsons
Thomas J. Sharpton
Stephen J. Giovannoni
Identification of rare microbial colonizers of plastic materials incubated in a coral reef environment
Frontiers in Microbiology
plastisphere
microbiome
polyolefins
microbial succession
in situ
16S rDNA
title Identification of rare microbial colonizers of plastic materials incubated in a coral reef environment
title_full Identification of rare microbial colonizers of plastic materials incubated in a coral reef environment
title_fullStr Identification of rare microbial colonizers of plastic materials incubated in a coral reef environment
title_full_unstemmed Identification of rare microbial colonizers of plastic materials incubated in a coral reef environment
title_short Identification of rare microbial colonizers of plastic materials incubated in a coral reef environment
title_sort identification of rare microbial colonizers of plastic materials incubated in a coral reef environment
topic plastisphere
microbiome
polyolefins
microbial succession
in situ
16S rDNA
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1259014/full
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