Evidence That Microorganisms at the Animal-Water Interface Drive Sea Star Wasting Disease

Sea star wasting (SSW) disease describes a condition affecting asteroids that resulted in significant Northeastern Pacific population decline following a mass mortality event in 2013. The etiology of SSW is unresolved. We hypothesized that SSW is a sequela of microbial organic matter remineralizatio...

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Main Authors: Citlalli A. Aquino, Ryan M. Besemer, Christopher M. DeRito, Jan Kocian, Ian R. Porter, Peter T. Raimondi, Jordan E. Rede, Lauren M. Schiebelhut, Jed P. Sparks, John P. Wares, Ian Hewson
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-01-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2020.610009/full
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spelling doaj-e670784e53bc439aa35475eee890f7b32021-01-06T04:56:14ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-01-011110.3389/fmicb.2020.610009610009Evidence That Microorganisms at the Animal-Water Interface Drive Sea Star Wasting DiseaseCitlalli A. Aquino0Ryan M. Besemer1Christopher M. DeRito2Jan Kocian3Ian R. Porter4Peter T. Raimondi5Jordan E. Rede6Lauren M. Schiebelhut7Jed P. Sparks8John P. Wares9Ian Hewson10Department of Biology, Estuary and Ocean Science Center, San Francisco State University, Tiburon, CA, United StatesCenter for Marine Science, University of North Carolina Wilmington, Wilmington, NC, United StatesDepartment of Microbiology, Cornell University, Ithaca, NY, United StatesUnaffiliated Researcher, Freeland, WA, United StatesDepartment of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY, United StatesInstitute of Marine Sciences, Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, Santa Cruz, CA, United StatesDepartment of Microbiology, Cornell University, Ithaca, NY, United StatesLife and Environmental Sciences, University of California, Merced, Merced, CA, United StatesDepartment of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, United StatesDepartment of Genetics, University of Georgia, Athens, GA, United StatesDepartment of Microbiology, Cornell University, Ithaca, NY, United StatesSea star wasting (SSW) disease describes a condition affecting asteroids that resulted in significant Northeastern Pacific population decline following a mass mortality event in 2013. The etiology of SSW is unresolved. We hypothesized that SSW is a sequela of microbial organic matter remineralization near respiratory surfaces, one consequence of which may be limited O2 availability at the animal-water interface. Microbial assemblages inhabiting tissues and at the asteroid-water interface bore signatures of copiotroph proliferation before SSW onset, followed by the appearance of putatively facultative and strictly anaerobic taxa at the time of lesion genesis and as animals died. SSW lesions were induced in Pisaster ochraceus by enrichment with a variety of organic matter (OM) sources. These results together illustrate that depleted O2 conditions at the animal-water interface may be established by heterotrophic microbial activity in response to organic matter loading. SSW was also induced by modestly (∼39%) depleted O2 conditions in aquaria, suggesting that small perturbations in dissolved O2 may exacerbate the condition. SSW susceptibility between species was significantly and positively correlated with surface rugosity, a key determinant of diffusive boundary layer thickness. Tissues of SSW-affected individuals collected in 2013–2014 bore δ15N signatures reflecting anaerobic processes, which suggests that this phenomenon may have affected asteroids during mass mortality at the time. The impacts of enhanced microbial activity and subsequent O2 diffusion limitation may be more pronounced under higher temperatures due to lower O2 solubility, in more rugose asteroid species due to restricted hydrodynamic flow, and in larger specimens due to their lower surface area to volume ratios which affects diffusive respiratory potential.https://www.frontiersin.org/articles/10.3389/fmicb.2020.610009/fullsea star wastingoxygenheterotrophremineralizationphytoplankton
collection DOAJ
language English
format Article
sources DOAJ
author Citlalli A. Aquino
Ryan M. Besemer
Christopher M. DeRito
Jan Kocian
Ian R. Porter
Peter T. Raimondi
Jordan E. Rede
Lauren M. Schiebelhut
Jed P. Sparks
John P. Wares
Ian Hewson
spellingShingle Citlalli A. Aquino
Ryan M. Besemer
Christopher M. DeRito
Jan Kocian
Ian R. Porter
Peter T. Raimondi
Jordan E. Rede
Lauren M. Schiebelhut
Jed P. Sparks
John P. Wares
Ian Hewson
Evidence That Microorganisms at the Animal-Water Interface Drive Sea Star Wasting Disease
Frontiers in Microbiology
sea star wasting
oxygen
heterotroph
remineralization
phytoplankton
author_facet Citlalli A. Aquino
Ryan M. Besemer
Christopher M. DeRito
Jan Kocian
Ian R. Porter
Peter T. Raimondi
Jordan E. Rede
Lauren M. Schiebelhut
Jed P. Sparks
John P. Wares
Ian Hewson
author_sort Citlalli A. Aquino
title Evidence That Microorganisms at the Animal-Water Interface Drive Sea Star Wasting Disease
title_short Evidence That Microorganisms at the Animal-Water Interface Drive Sea Star Wasting Disease
title_full Evidence That Microorganisms at the Animal-Water Interface Drive Sea Star Wasting Disease
title_fullStr Evidence That Microorganisms at the Animal-Water Interface Drive Sea Star Wasting Disease
title_full_unstemmed Evidence That Microorganisms at the Animal-Water Interface Drive Sea Star Wasting Disease
title_sort evidence that microorganisms at the animal-water interface drive sea star wasting disease
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2021-01-01
description Sea star wasting (SSW) disease describes a condition affecting asteroids that resulted in significant Northeastern Pacific population decline following a mass mortality event in 2013. The etiology of SSW is unresolved. We hypothesized that SSW is a sequela of microbial organic matter remineralization near respiratory surfaces, one consequence of which may be limited O2 availability at the animal-water interface. Microbial assemblages inhabiting tissues and at the asteroid-water interface bore signatures of copiotroph proliferation before SSW onset, followed by the appearance of putatively facultative and strictly anaerobic taxa at the time of lesion genesis and as animals died. SSW lesions were induced in Pisaster ochraceus by enrichment with a variety of organic matter (OM) sources. These results together illustrate that depleted O2 conditions at the animal-water interface may be established by heterotrophic microbial activity in response to organic matter loading. SSW was also induced by modestly (∼39%) depleted O2 conditions in aquaria, suggesting that small perturbations in dissolved O2 may exacerbate the condition. SSW susceptibility between species was significantly and positively correlated with surface rugosity, a key determinant of diffusive boundary layer thickness. Tissues of SSW-affected individuals collected in 2013–2014 bore δ15N signatures reflecting anaerobic processes, which suggests that this phenomenon may have affected asteroids during mass mortality at the time. The impacts of enhanced microbial activity and subsequent O2 diffusion limitation may be more pronounced under higher temperatures due to lower O2 solubility, in more rugose asteroid species due to restricted hydrodynamic flow, and in larger specimens due to their lower surface area to volume ratios which affects diffusive respiratory potential.
topic sea star wasting
oxygen
heterotroph
remineralization
phytoplankton
url https://www.frontiersin.org/articles/10.3389/fmicb.2020.610009/full
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