A Three-Stage Symbiosis Forms the Foundation of Seagrass Ecosystems

Heide, Tjisse van der; Govers, Laura L.; Fouw, Jimmy de; Olff, Han; Geest, Matthijs van der; Katwijk, M.M. van; Piersma, Theunis; Koppel, Johan van de; Silliman, Brian R.; Smolders, Alfons J. P.; Gils, Jan A. van

doi:10.1126/science.1219973

Cited by 225 publications

(217 citation statements)

References 72 publications

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“…In particular, organic matter accumulation within coastal sediments causes sediment sulfide conditions that are toxic for vascular plants (40)(41)(42). The most abundant of the root-enriched microbial taxa detected in this study clustered within the genus Sulfurimonas, which accounted for ca.…”

Section: Discussionmentioning

confidence: 94%

Global-scale structure of the eelgrass microbiome

Fahimipour

Kardish

Eisen

et al. 2016

Preprint

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Plant-associated microorganisms are essential for their hosts' survival and performance. Yet, most plant microbiome studies to date have focused on terrestrial species sampled across relatively small spatial scales. Here, we report the results of a global-scale analysis of microbial communities associated with leaf and root surfaces of the marine eelgrass Zostera marina throughout its range in the Northern Hemisphere. By contrasting host microbiomes with those of surrounding seawater and sediment, we uncovered the structure, composition, and variability of microbial communities associated with eelgrass. We also investigated hypotheses about the assembly of the eelgrass microbiome using a metabolic modeling approach. Our results reveal leaf communities displaying high variability and spatial turnover that mirror their adjacent coastal seawater microbiomes. By contrast, roots showed relatively low compositional turnover and were distinct from surrounding sediment communities, a result driven by the enrichment of predicted sulfur-oxidizing bacterial taxa on root surfaces. Predictions from metabolic modeling of enriched taxa were consistent with a habitat-filtering community assembly mechanism whereby similarity in resource use drives taxonomic cooccurrence patterns on belowground, but not aboveground, host tissues. Our work provides evidence for a core eelgrass root microbiome with putative functional roles and highlights potentially disparate processes influencing microbial community assembly on different plant compartments.IMPORTANCE Plants depend critically on their associated microbiome, yet the structure of microbial communities found on marine plants remains poorly understood in comparison to that for terrestrial species. Seagrasses are the only flowering plants that live entirely in marine environments. The return of terrestrial seagrass ancestors to oceans is among the most extreme habitat shifts documented in plants, making them an ideal testbed for the study of microbial symbioses with plants that experience relatively harsh abiotic conditions. In this study, we report the results of a global sampling effort to extensively characterize the structure of microbial communities associated with the widespread seagrass species Zostera marina, or eelgrass, across its geographic range. Our results reveal major differences in the structure and composition of above-versus belowground microbial communities on eelgrass surfaces, as well as their relationships with the environment and host.

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Section: Discussionmentioning

confidence: 94%

Global-scale structure of the eelgrass microbiome

Fahimipour

Kardish

Eisen

et al. 2016

Preprint

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“…The long habitat cascade in the Avon‐Heathcote Estuary could therefore be expanded to have yet another basal layer in places where Zostera provides habitat for Austrovenus (see experiments 1 and 3). Similar patterns of coexistence between seagrass and embedded shell‐forming molluscs have been reported from around the world (van der Heide et al., 2012). …”

Section: Discussionmentioning

confidence: 99%

A sixth‐level habitat cascade increases biodiversity in an intertidal estuary

Thomsen

Hildebrand

South

et al. 2016

Ecology and Evolution

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Many studies have documented habitat cascades where two co‐occurring habitat‐forming species control biodiversity. However, more than two habitat‐formers could theoretically co‐occur. We here documented a sixth‐level habitat cascade from the Avon‐Heathcote Estuary, New Zealand, by correlating counts of attached inhabitants to the size and accumulated biomass of their biogenic hosts. These data revealed predictable sequences of habitat‐formation (=attachment space). First, the bivalve Austrovenus provided habitat for green seaweeds (Ulva) that provided habitat for trochid snails in a typical estuarine habitat cascade. However, the trochids also provided habitat for the nonnative bryozoan Conopeum that provided habitat for the red seaweed Gigartina that provided habitat for more trochids, thereby resetting the sequence of the habitat cascade, theoretically in perpetuity. Austrovenus is here the basal habitat‐former that controls this “long” cascade. The strength of facilitation increased with seaweed frond size, accumulated seaweed biomass, accumulated shell biomass but less with shell size. We also found that Ulva attached to all habitat‐formers, trochids attached to Ulva and Gigartina, and Conopeum and Gigartina predominately attached to trochids. These “affinities” for different habitat‐forming species probably reflect species‐specific traits of juveniles and adults. Finally, manipulative experiments confirmed that the amount of seaweed and trochids was important and consistent regulators of the habitat cascade in different estuarine environments. We also interpreted this cascade as a habitat‐formation network that describes the likelihood of an inhabitant being found attached to a specific habitat‐former. We conclude that the strength of the cascade increased with the amount of higher‐order habitat‐formers, with differences in form and function between higher and lower‐order habitat‐formers, and with the affinity of inhabitants for higher‐order habitat‐formers. We suggest that long habitat cascades are common where species traits allow for physical attachment to other species, such as in marine benthic systems and old forest.

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“…Additionally, decomposition of macroalgae mats may decrease oxygen content in eutrophicated waters and further abate seagrass survival (McGlathery et al, 2007). Furthermore, high sulfide concentration due to the anoxia from macroalgae decomposition can decrease the photosynthetic rate of seagrasses, reducing growth and even resulting in mortality (Holmer and Nielsen, 2007;Koch et al, 2007;Pedersen et al, 2004;van der Heide et al, 2012). With average temperatures rising on a global scale, blooms of green algae such as Ulva pertusa may be expected to increase (Sousa-Dias and Melo, 2008), which could in turn further increase the competitive advantage of green algae over some seagrasses (Koch et al, 2013 and references therein).…”

Section: Introductionmentioning

confidence: 99%

Combined nutrient and macroalgae loads lead to response in seagrass indicator properties

Han

Soissons

Bouma

et al. 2016

Marine Pollution Bulletin

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a b s t r a c t a r t i c l e i n f oExcess nutrients are potential factors that drive phase shifts from seagrasses to macroalgae. We carried out a manipulative field experiment to study the effects of macroalgae Ulva pertusa loading and nutrient addition to the water column on the nitrogen (N) and carbon (C) contents (i.e., fast indicators) as well as on the morphology and structure (i.e., slow indicators) of Zostera marina. Our results showed rapid impact of increased macroalgae and nutrient load on Z. marina C/N ratios. Also, macroalgae addition resulted in a trend of decreasing belowground biomass of seagrasses, and nutrient load significantly decreased above to belowground biomass ratio. Although some morphological/structural variables showed relatively fast responses, the effects of short-term disturbance by macroalgae and nutrients were less often significant than on physiological variables. Monitoring of seagrass physiological indicators may allow for early detection of eutrophication, which may initiate timely management interventions to avert seagrass loss.

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A Three-Stage Symbiosis Forms the Foundation of Seagrass Ecosystems

Cited by 225 publications

References 72 publications

Global-scale structure of the eelgrass microbiome

Global-scale structure of the eelgrass microbiome

A sixth‐level habitat cascade increases biodiversity in an intertidal estuary

Combined nutrient and macroalgae loads lead to response in seagrass indicator properties

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