Algicidal and growth-inhibiting bacteria associated with seagrass and macroalgae beds in Puget Sound, WA, USA

Inaba, Nobuharu; Trainer, Vera L.; Onishi, Yuka; Ishii, Kenichiro; Wyllie‐Echeverria, Sandy; Imai, Ichiro

doi:10.1016/j.hal.2016.04.004

Cited by 52 publications

(39 citation statements)

References 42 publications

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“…These results 51 extend previous evidence for an allelopathy of Z. marina (and/or associated taxa) towards 52 particular harmful algal bloom (HAB) species that cause paralytic or diarrhetic shellfish 53 poisoning (e.g. Inaba et al, 2017), by demonstrating an effect of eelgrass communities on 54 dinoflagellates in a 'halo' of influence surrounding the habitat. In the region of study, toxigenic 55 dinoflagellate distributions have expanded over time, and are associated with an increase in the 56 number of shellfish harvesting closures (Trainer et al, 2003;Moore et al, 2009).…”

Section: Introduction 23supporting

confidence: 67%

A Halo of Reduced Dinoflagellate Abundances In and Around Eelgrass Beds

Jacobs-Palmer

Gallego

Ramón-Laca

et al. 2019

Preprint

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ABSTRACTSeagrass beds provide a variety of ecosystem services, both within and outside the bounds of the habitat itself. Here we use environmental DNA (eDNA) amplicons to analyze a broad cross-section of taxa from ecological communities in and immediately surrounding eelgrass (Zostera marina). Sampling seawater along transects extending alongshore outward from eelgrass beds, we demonstrate that eDNA provides meter-scale resolution of communities in the field. We evaluate eDNA abundance indices for thirteen major phylogenetic groups of marine and estuarine taxa along these transects, finding highly local changes linked with proximity to Z. marina for a diverse group of dinoflagellates, and for no other group of taxa. Eelgrass habitat is consistently associated with dramatic reductions in dinoflagellate abundance both within the contiguous beds and for at least fifteen meters outside, relative to nearby sites without eelgrass. These results are consistent with the hypothesis that eelgrass-associated communities have allelopathic effects on dinoflagellates, and that these effects can extend in a halo beyond the bounds of the contiguous beds. Because many dinoflagellates are capable of forming Harmful Algal Blooms (HABs) toxic to humans and other animal species, the apparent salutary effect of eelgrass habitat on neighboring waters has important implications for public health as well as shellfish aquaculture and harvesting.

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Section: Introduction 23supporting

confidence: 67%

A Halo of Reduced Dinoflagellate Abundances In and Around Eelgrass Beds

Jacobs-Palmer

Gallego

Ramón-Laca

et al. 2019

Preprint

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“…A specific allelopathy against microalgal species by Z. marina was first described over 30 years ago (Harrison & Durance, 1985). More recent evidence suggests this negative interaction applies to multiple HAB taxa that cause paralytic or diarrhetic shellfish poisoning (including Alexandrium, a genus observed in this study), and is mediated locally by a variety of strains of eelgrass-associated algicidal and growth-inhibiting bacteria, particularly from Erythrobacter, Teredinibacter, Gaetbulibacter and Arthrobacter genera (Inaba et al, 2017) (though the eDNA primers employed here amplify eukaryotes almost exclusively and therefore do not allow us to test this mechanism). However, in our dataset the repressive effect of eelgrass notably does not extend at the phylum level to other phytoplankton such as diatoms (Bacillariophyta) and green algae (Chlorophyta), despite reports that Z. marina habitat can deter members of these taxa as well (reviewed in Gross (2003)).…”

Section: Discussionmentioning

confidence: 51%

“…Additionally, seagrass tissue itself is a source of diverse secondary metabolites capable of killing bacteria responsible for a variety of serious infections (Kannan, Arumugam & Anantharaman, 2010;reviewed in Zidorn (2016)). Finally, specific bacteria associated with seagrasses are known to kill or inhibit the growth of taxa that produce harmful algal blooms (HABs) (Inaba et al, 2017; reviewed in Imai (2015)), which can cause shellfish poisoning, fish kills, and mass de-oxygenation events, among other detrimental effects (reviewed in Grattan, Holobaugh & Morris (2016), Hallegraeff et al (2017) and Rabalais et al (2014), respectively). Thus, the antimicrobial properties of seagrass and associated organisms also yield benefits for human and local ecosystem health.…”

Section: Introductionmentioning

confidence: 99%

A halo of reduced dinoflagellate abundances in and around eelgrass beds

Jacobs-Palmer

Gallego

Ramón-Laca

et al. 2020

PeerJ

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Seagrass beds provide a variety of ecosystem services, both within and outside the bounds of the habitat itself. Here we use environmental DNA (eDNA) amplicons to analyze a broad cross-section of taxa from ecological communities in and immediately surrounding eelgrass (Zostera marina). Sampling seawater along transects extending alongshore outward from eelgrass beds, we demonstrate that eDNA provides meter-scale resolution of communities in the field. We evaluate eDNA abundance indices for 13 major phylogenetic groups of marine and estuarine taxa along these transects, finding highly local changes linked with proximity to Z. marina for a diverse group of dinoflagellates, and for no other group of taxa. Eelgrass habitat is consistently associated with dramatic reductions in dinoflagellate abundance both within the contiguous beds and for at least 15 m outside, relative to nearby sites without eelgrass. These results are consistent with the hypothesis that eelgrass-associated communities have allelopathic effects on dinoflagellates, and that these effects can extend in a halo beyond the bounds of the contiguous beds. Because many dinoflagellates are capable of forming harmful algal blooms (HABs) toxic to humans and other animal species, the apparent salutary effect of eelgrass habitat on neighboring waters has important implications for public health as well as shellfish aquaculture and harvesting.

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“…Bacteria utilize these carbon and energy inputs to fuel growth and, in turn, modify the microbial community in the water column (Clasen & Shurin, 2014;Egan et al, 2013;Lam, Stang, & Harder, 2008;Linley, Newell, & Bosma, 1981;Stuart et al, 1981) and on nearby biofilms (Fischer, Friedrichs, & Lachnit, 2014;Vega Thurber et al, 2012;Zaneveld et al, 2016). Macroalgae also release a variety of antimicrobial compounds into the water that can inhibit growth of particular bacteria, fungi and algae (Dahms & Dobretsov, 2017;Inaba et al, 2017;Lam & Harder, 2007;Lam et al, 2008). Finally, macroalgae modify the microbiota in their surroundings through the dispersal of epibiotic microbes directly into the water column or on particles of degrading algal tissue.…”

mentioning

confidence: 99%

Incubation with macroalgae induces large shifts in water column microbiota, but minor changes to the epibiota of co‐occurring macroalgae

Chen

Parfrey

2018

Molecular Ecology

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Macroalgae variably promote and deter microbial growth through release of organic carbon and antimicrobial compounds into the water column. Consequently, macroalgae influence the microbial composition of the surrounding water column and biofilms on nearby surfaces. Here, we use manipulative experiments to test the hypotheses that (i) Nereocystis luetkeana and Mastocarpus sp. macroalgae alter the water column microbiota in species-specific manner, that (ii) neighbouring macroalgae alter the bacterial communities on the surface (epibiota) of actively growing Nereocystis luetkeana meristem fragments (NMFs), and that (iii) neighbours alter NMF growth rate. We also assess the impact of laboratory incubation on macroalgal epibiota by comparing each species to wild counterparts. We find strong differences between the Nereocystis and Mastocarpus epibiota that are maintained in the laboratory. Nereocystis and Mastocarpus alter water column bacterial community composition and richness in a species specific manner, but cause only small compositional shifts on NMF surfaces that do not differ by species, and do not change richness. Co-incubation with macroalgae results in significant change in abundance of fivefold more genera in the water column compared to NMF surfaces, although the direction (i.e., enrichment or reduction) of shift is generally consistent between the water and NMF surfaces. Finally, NMFs grew during the experiment, but growth did not depend on the presence or identity of neighbouring macroalgae. Thus, macroalgae exhibit a strong and species-specific influence on the water column microbiota, but a much weaker influence on the epibiota of neighbouring macroalgae. Overall, these results support the idea that macroalgae surfaces are highly selective and demonstrate that modulations of macroalgal microbiota operate within an overarching paradigm of host species specificity.

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Algicidal and growth-inhibiting bacteria associated with seagrass and macroalgae beds in Puget Sound, WA, USA

Cited by 52 publications

References 42 publications

A Halo of Reduced Dinoflagellate Abundances In and Around Eelgrass Beds

A Halo of Reduced Dinoflagellate Abundances In and Around Eelgrass Beds

A halo of reduced dinoflagellate abundances in and around eelgrass beds

Incubation with macroalgae induces large shifts in water column microbiota, but minor changes to the epibiota of co‐occurring macroalgae

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