Metal-macrofauna interactions determine microbial community structure and function in copper contaminated sediments

Daniel J Mayor, Nia B Gray, Joanna Elver-Evans, Andrew J Midwood, Barry Thornton

Research output: Contribution to journalArticle

22 Citations (Scopus)
3 Downloads (Pure)

Abstract

Copper is essential for healthy cellular functioning, but this heavy metal quickly becomes toxic when supply exceeds demand. Marine sediments receive widespread and increasing levels of copper contamination from antifouling paints owing to the 2008 global ban of organotin-based products. The toxicity of copper will increase in the coming years as seawater pH decreases and temperature increases. We used a factorial mesocosm experiment to investigate how increasing sediment copper concentrations and the presence of a cosmopolitan bioturbating amphipod, Corophium volutator, affected a range of ecosystem functions in a soft sediment microbial community. The effects of copper on benthic nutrient release, bacterial biomass, microbial community structure and the isotopic composition of individual microbial membrane [phospholipid] fatty acids (PLFAs) all differed in the presence of C. volutator. Our data consistently demonstrate that copper contamination of global waterways will have pervasive effects on the metabolic functioning of benthic communities that cannot be predicted from copper concentrations alone; impacts will depend upon the resident macrofauna and their capacity for bioturbation. This finding poses a major challenge for those attempting to manage the impacts of copper contamination on ecosystem services, e.g. carbon and nutrient cycling, across different habitats. Our work also highlights the paucity of information on the processes that result in isotopic fractionation in natural marine microbial communities. We conclude that the assimilative capacity of benthic microbes will become progressively impaired as copper concentrations increase. These effects will, to an extent, be mitigated by the presence of bioturbating animals and possibly other processes that increase the influx of oxygenated seawater into the sediments. Our findings support the move towards an ecosystem approach for environmental management.
Original languageEnglish
Article numbere64940
Number of pages9
JournalPloS ONE
Volume8
Issue number5
DOIs
Publication statusPublished - 31 May 2013

Fingerprint

Microbial Interactions
microbial communities
Copper
Sediments
community structure
copper
Metals
metals
sediments
Ecosystem
Ecosystems
Contamination
Seawater
Nutrients
seawater
Antifouling paint
Amphipoda
Geologic Sediments
isotope fractionation
Food

Cite this

Metal-macrofauna interactions determine microbial community structure and function in copper contaminated sediments. / Mayor, Daniel J; Gray, Nia B; Elver-Evans, Joanna; Midwood, Andrew J; Thornton, Barry.

In: PloS ONE, Vol. 8, No. 5, e64940, 31.05.2013.

Research output: Contribution to journalArticle

Mayor, Daniel J ; Gray, Nia B ; Elver-Evans, Joanna ; Midwood, Andrew J ; Thornton, Barry. / Metal-macrofauna interactions determine microbial community structure and function in copper contaminated sediments. In: PloS ONE. 2013 ; Vol. 8, No. 5.
@article{f7615a2e2ce64fb48be9d461c74732b4,
title = "Metal-macrofauna interactions determine microbial community structure and function in copper contaminated sediments",
abstract = "Copper is essential for healthy cellular functioning, but this heavy metal quickly becomes toxic when supply exceeds demand. Marine sediments receive widespread and increasing levels of copper contamination from antifouling paints owing to the 2008 global ban of organotin-based products. The toxicity of copper will increase in the coming years as seawater pH decreases and temperature increases. We used a factorial mesocosm experiment to investigate how increasing sediment copper concentrations and the presence of a cosmopolitan bioturbating amphipod, Corophium volutator, affected a range of ecosystem functions in a soft sediment microbial community. The effects of copper on benthic nutrient release, bacterial biomass, microbial community structure and the isotopic composition of individual microbial membrane [phospholipid] fatty acids (PLFAs) all differed in the presence of C. volutator. Our data consistently demonstrate that copper contamination of global waterways will have pervasive effects on the metabolic functioning of benthic communities that cannot be predicted from copper concentrations alone; impacts will depend upon the resident macrofauna and their capacity for bioturbation. This finding poses a major challenge for those attempting to manage the impacts of copper contamination on ecosystem services, e.g. carbon and nutrient cycling, across different habitats. Our work also highlights the paucity of information on the processes that result in isotopic fractionation in natural marine microbial communities. We conclude that the assimilative capacity of benthic microbes will become progressively impaired as copper concentrations increase. These effects will, to an extent, be mitigated by the presence of bioturbating animals and possibly other processes that increase the influx of oxygenated seawater into the sediments. Our findings support the move towards an ecosystem approach for environmental management.",
author = "Mayor, {Daniel J} and Gray, {Nia B} and Joanna Elver-Evans and Midwood, {Andrew J} and Barry Thornton",
year = "2013",
month = "5",
day = "31",
doi = "10.1371/journal.pone.0064940",
language = "English",
volume = "8",
journal = "PloS ONE",
issn = "1932-6203",
publisher = "PUBLIC LIBRARY SCIENCE",
number = "5",

}

TY - JOUR

T1 - Metal-macrofauna interactions determine microbial community structure and function in copper contaminated sediments

AU - Mayor, Daniel J

AU - Gray, Nia B

AU - Elver-Evans, Joanna

AU - Midwood, Andrew J

AU - Thornton, Barry

PY - 2013/5/31

Y1 - 2013/5/31

N2 - Copper is essential for healthy cellular functioning, but this heavy metal quickly becomes toxic when supply exceeds demand. Marine sediments receive widespread and increasing levels of copper contamination from antifouling paints owing to the 2008 global ban of organotin-based products. The toxicity of copper will increase in the coming years as seawater pH decreases and temperature increases. We used a factorial mesocosm experiment to investigate how increasing sediment copper concentrations and the presence of a cosmopolitan bioturbating amphipod, Corophium volutator, affected a range of ecosystem functions in a soft sediment microbial community. The effects of copper on benthic nutrient release, bacterial biomass, microbial community structure and the isotopic composition of individual microbial membrane [phospholipid] fatty acids (PLFAs) all differed in the presence of C. volutator. Our data consistently demonstrate that copper contamination of global waterways will have pervasive effects on the metabolic functioning of benthic communities that cannot be predicted from copper concentrations alone; impacts will depend upon the resident macrofauna and their capacity for bioturbation. This finding poses a major challenge for those attempting to manage the impacts of copper contamination on ecosystem services, e.g. carbon and nutrient cycling, across different habitats. Our work also highlights the paucity of information on the processes that result in isotopic fractionation in natural marine microbial communities. We conclude that the assimilative capacity of benthic microbes will become progressively impaired as copper concentrations increase. These effects will, to an extent, be mitigated by the presence of bioturbating animals and possibly other processes that increase the influx of oxygenated seawater into the sediments. Our findings support the move towards an ecosystem approach for environmental management.

AB - Copper is essential for healthy cellular functioning, but this heavy metal quickly becomes toxic when supply exceeds demand. Marine sediments receive widespread and increasing levels of copper contamination from antifouling paints owing to the 2008 global ban of organotin-based products. The toxicity of copper will increase in the coming years as seawater pH decreases and temperature increases. We used a factorial mesocosm experiment to investigate how increasing sediment copper concentrations and the presence of a cosmopolitan bioturbating amphipod, Corophium volutator, affected a range of ecosystem functions in a soft sediment microbial community. The effects of copper on benthic nutrient release, bacterial biomass, microbial community structure and the isotopic composition of individual microbial membrane [phospholipid] fatty acids (PLFAs) all differed in the presence of C. volutator. Our data consistently demonstrate that copper contamination of global waterways will have pervasive effects on the metabolic functioning of benthic communities that cannot be predicted from copper concentrations alone; impacts will depend upon the resident macrofauna and their capacity for bioturbation. This finding poses a major challenge for those attempting to manage the impacts of copper contamination on ecosystem services, e.g. carbon and nutrient cycling, across different habitats. Our work also highlights the paucity of information on the processes that result in isotopic fractionation in natural marine microbial communities. We conclude that the assimilative capacity of benthic microbes will become progressively impaired as copper concentrations increase. These effects will, to an extent, be mitigated by the presence of bioturbating animals and possibly other processes that increase the influx of oxygenated seawater into the sediments. Our findings support the move towards an ecosystem approach for environmental management.

UR - http://www.scopus.com/inward/record.url?scp=84878590565&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0064940

DO - 10.1371/journal.pone.0064940

M3 - Article

VL - 8

JO - PloS ONE

JF - PloS ONE

SN - 1932-6203

IS - 5

M1 - e64940

ER -