Mud, Microbes, and Macrofauna: Seasonal Dynamics of the Iron Biogeochemical Cycle in an Intertidal Mudflat

Microorganisms and burrowing animals exert a pronounced impact on the cycling of redox sensitive metals in coastal sediments. We hypothesized that the iron biogeochemical cycle and associated sedimentary microbial community will respond to seasonal changes in a bioturbated intertidal mudflat. In thi...

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Main Authors: Jacob P. Beam, Sarabeth George, Nicholas R. Record, Peter D. Countway, David T. Johnston, Peter R. Girguis, David Emerson
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-11-01
Series:Frontiers in Marine Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmars.2020.562617/full
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spelling doaj-e4f70e9a593e4605809ee4b381b4cb392020-11-25T04:10:32ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452020-11-01710.3389/fmars.2020.562617562617Mud, Microbes, and Macrofauna: Seasonal Dynamics of the Iron Biogeochemical Cycle in an Intertidal MudflatJacob P. Beam0Sarabeth George1Sarabeth George2Nicholas R. Record3Peter D. Countway4David T. Johnston5Peter R. Girguis6David Emerson7Bigelow Laboratory for Ocean Sciences, Boothbay, ME, United StatesBigelow Laboratory for Ocean Sciences, Boothbay, ME, United StatesSan Francisco Bay Regional Water Quality Control Board, Oakland, CA, United StatesBigelow Laboratory for Ocean Sciences, Boothbay, ME, United StatesBigelow Laboratory for Ocean Sciences, Boothbay, ME, United StatesDepartment of Earth and Planetary Sciences, Harvard University, Cambridge, MA, United StatesDepartment of Organismal and Evolutionary Biology, Harvard University, Cambridge, MA, United StatesBigelow Laboratory for Ocean Sciences, Boothbay, ME, United StatesMicroorganisms and burrowing animals exert a pronounced impact on the cycling of redox sensitive metals in coastal sediments. We hypothesized that the iron biogeochemical cycle and associated sedimentary microbial community will respond to seasonal changes in a bioturbated intertidal mudflat. In this study, we monitored the spatiotemporal dynamics of porewater and highly reactive solid phase iron with the corresponding prokaryotic and eukaryotic sedimentary microbial communities over one annual cycle from November 2015 to November 2016. Continuous and seasonally variable pools of both porewater Fe(II) and highly reactive iron (FeHR) were observed throughout the seasons with significant increases of Fe(II) and FeHR in response to increased sediment temperature in summer months. Maximum concentrations of Fe(II) and FeHR were predominantly confined to the upper 5 cm of sediment throughout the year. Iron-oxidizing and -reducing microorganisms were present and stable temporally, and exhibited a depth-dependent stratification likely due to availability of Fe(II) and FeHR pools, respectively. Zetaproteobacteria, presumptive lithotrophic iron-oxidizing bacteria, were present at abundances around 0.5–1% in the top 5 cm of sediment with decline abundance with depth. As a whole the microbial community was relatively stable across the seasons, and showed strongest separation with depth, probably driven by changes in oxygen availability and organic matter. The Deltaproteobacteria, principally taxa known to be associated with sulfur and iron cycling, were prevalent, especially at >5 cm depth. Gammaproteobacteria and Bacteroidetes were also abundant, with putatively aerobic members especially prevalent in the cm of the sediment. The relative abundance of diatoms, estimated from abundance of 18S rRNA gene counts, showed evidence of a seasonal signal possibly tied to spring and fall blooms. Overall, analysis of phytoplankton found significant abundance at depth, likely due to the feeding and bio-mixing activity of marine worms. Macro-, and meiofauna, consistent with expected taxa, were detected throughout the year via 18S gene counts, and showed some seasonal variations that may influence sedimentary iron transformations by active microbial grazing. In summary, this analysis revealed relatively consistent temporal and spatial trends in iron geochemistry and microbial and macrobial community composition, while also indicating a complex dynamic of microbial and macrobial interactions are responsible for maintaining these processes.https://www.frontiersin.org/articles/10.3389/fmars.2020.562617/fullferrous ironmarine sedimentiron cyclebioturbationZetaproteobacteria
collection DOAJ
language English
format Article
sources DOAJ
author Jacob P. Beam
Sarabeth George
Sarabeth George
Nicholas R. Record
Peter D. Countway
David T. Johnston
Peter R. Girguis
David Emerson
spellingShingle Jacob P. Beam
Sarabeth George
Sarabeth George
Nicholas R. Record
Peter D. Countway
David T. Johnston
Peter R. Girguis
David Emerson
Mud, Microbes, and Macrofauna: Seasonal Dynamics of the Iron Biogeochemical Cycle in an Intertidal Mudflat
Frontiers in Marine Science
ferrous iron
marine sediment
iron cycle
bioturbation
Zetaproteobacteria
author_facet Jacob P. Beam
Sarabeth George
Sarabeth George
Nicholas R. Record
Peter D. Countway
David T. Johnston
Peter R. Girguis
David Emerson
author_sort Jacob P. Beam
title Mud, Microbes, and Macrofauna: Seasonal Dynamics of the Iron Biogeochemical Cycle in an Intertidal Mudflat
title_short Mud, Microbes, and Macrofauna: Seasonal Dynamics of the Iron Biogeochemical Cycle in an Intertidal Mudflat
title_full Mud, Microbes, and Macrofauna: Seasonal Dynamics of the Iron Biogeochemical Cycle in an Intertidal Mudflat
title_fullStr Mud, Microbes, and Macrofauna: Seasonal Dynamics of the Iron Biogeochemical Cycle in an Intertidal Mudflat
title_full_unstemmed Mud, Microbes, and Macrofauna: Seasonal Dynamics of the Iron Biogeochemical Cycle in an Intertidal Mudflat
title_sort mud, microbes, and macrofauna: seasonal dynamics of the iron biogeochemical cycle in an intertidal mudflat
publisher Frontiers Media S.A.
series Frontiers in Marine Science
issn 2296-7745
publishDate 2020-11-01
description Microorganisms and burrowing animals exert a pronounced impact on the cycling of redox sensitive metals in coastal sediments. We hypothesized that the iron biogeochemical cycle and associated sedimentary microbial community will respond to seasonal changes in a bioturbated intertidal mudflat. In this study, we monitored the spatiotemporal dynamics of porewater and highly reactive solid phase iron with the corresponding prokaryotic and eukaryotic sedimentary microbial communities over one annual cycle from November 2015 to November 2016. Continuous and seasonally variable pools of both porewater Fe(II) and highly reactive iron (FeHR) were observed throughout the seasons with significant increases of Fe(II) and FeHR in response to increased sediment temperature in summer months. Maximum concentrations of Fe(II) and FeHR were predominantly confined to the upper 5 cm of sediment throughout the year. Iron-oxidizing and -reducing microorganisms were present and stable temporally, and exhibited a depth-dependent stratification likely due to availability of Fe(II) and FeHR pools, respectively. Zetaproteobacteria, presumptive lithotrophic iron-oxidizing bacteria, were present at abundances around 0.5–1% in the top 5 cm of sediment with decline abundance with depth. As a whole the microbial community was relatively stable across the seasons, and showed strongest separation with depth, probably driven by changes in oxygen availability and organic matter. The Deltaproteobacteria, principally taxa known to be associated with sulfur and iron cycling, were prevalent, especially at >5 cm depth. Gammaproteobacteria and Bacteroidetes were also abundant, with putatively aerobic members especially prevalent in the cm of the sediment. The relative abundance of diatoms, estimated from abundance of 18S rRNA gene counts, showed evidence of a seasonal signal possibly tied to spring and fall blooms. Overall, analysis of phytoplankton found significant abundance at depth, likely due to the feeding and bio-mixing activity of marine worms. Macro-, and meiofauna, consistent with expected taxa, were detected throughout the year via 18S gene counts, and showed some seasonal variations that may influence sedimentary iron transformations by active microbial grazing. In summary, this analysis revealed relatively consistent temporal and spatial trends in iron geochemistry and microbial and macrobial community composition, while also indicating a complex dynamic of microbial and macrobial interactions are responsible for maintaining these processes.
topic ferrous iron
marine sediment
iron cycle
bioturbation
Zetaproteobacteria
url https://www.frontiersin.org/articles/10.3389/fmars.2020.562617/full
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