The Prokaryotic and Eukaryotic Microbiome of Pacific Oyster Spat is Shaped by Ocean Warming but not Acidification

Zhong, Xu; Chan, Amy M.; Collicutt, Brenna; Daspe, Maxim; Finke, Jan F.; Foss, Megan; Green, Timothy J.; Harley, Christopher D. G.; Hesketh, Amelia V.; Miller, Kristina M.; Otto, Sarah P.; Rolheiser, Kate; Saunders, Rob; Sutherland, Ben J. G.; Suttle, Curtis A.

doi:10.1101/2023.07.07.548145

Cited by 3 publications

(1 citation statement)

References 117 publications

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“…In the present study the relative abundance of taxa in the core microbiome was significantly correlated to spat age (Figure 3). Similar shifts in microbiome composition with age have been documented in oysters from different life stages (33) and a recent study on the spat microbiome under experimental temperature and pCO2 stress also found a change of the microbiome composition with age (54). A correlation between the microbiome development and host age has also been documented in corals, insects and fish (41, 43, 55, 56).…”

Section: Discussionsupporting

confidence: 77%

The core microbiome of cultured Pacific oyster spat develops with age but not mortality

Cho,

Finke,

Zhong

et al. 2023

Preprint

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The Pacific oyster (Magallana gigas, also known as Crassostrea gigas) is the most widely cultured shellfish worldwide, but production has been affected by mortality events. This includes mortality events in hatcheries that can threaten the seed supply for growers. There are several pathogens that cause disease in oysters, but in many cases mortality events cannot be attributed to a single agent, and appear to be multifactorial and involve a combination of environmental variables, microbial interactions and disbiosis. In many organisms, a mature microbiome provides resilience against pathogens and environmental stressors. In this study we investigated the microbiomes of cohorts of freshly settled oyster spat, some of which experienced notable mortality. Deep sequencing of 16S rRNA gene fragments did not show a significant difference among the microbiomes of cohorts experiencing different levels of mortality, but revealed a characteristic core microbiome with 74 taxa. Irrespective of mortality, the spat core microbiomes changed significantly in the relative abundance of taxa as the spat aged; yet, remained distinct from the microbial community in the surrounding water. The core microbiome was dominated by bacteria in the families Rhodobacteraceae, Nitrosomonadaceae, Flavobacteriaceae, Pirellulaeceae and Saprospiraceae. Of these, 14 taxa were indicative for the change in the core microbiome, which we designated as the 'Hard-Core Microbiome'. The variability in diversity and richess of members of the core taxa decreased with oyster-spat aging, implying niche occupation. The study further accounts for the exchange of microbes with surrounding water during the core microbiome development. The observed shifts in the core microbiome with ageing oyster spat implies a crucial developmental period for the core microbiome of rearing spat.

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Section: Discussionsupporting

confidence: 77%

The core microbiome of cultured Pacific oyster spat develops with age but not mortality

Cho,

Finke,

Zhong

et al. 2023

Preprint

View full text Add to dashboard Cite

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The prokaryotic and eukaryotic microbiome of Pacific oyster spat is shaped by ocean warming but not acidification

Zhong,

Chan,

Collicutt

et al. 2024

Appl Environ Microbiol

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Pacific oysters ( Magallana gigas, a.k.a. Crassostrea gigas ), the most widely farmed oysters, are under threat from climate change and emerging pathogens. In part, their resilience may be affected by their microbiome, which, in turn, may be influenced by ocean warming and acidification. To understand these impacts, we exposed early-development Pacific oyster spat to different temperatures (18°C and 24°C) and p CO 2 levels (800, 1,600, and 2,800 µatm) in a fully crossed design for 3 weeks. Under all conditions, the microbiome changed over time, with a large decrease in the relative abundance of potentially pathogenic ciliates ( Uronema marinum ) in all treatments with time. The microbiome composition differed significantly with temperature, but not acidification, indicating that Pacific oyster spat microbiomes can be altered by ocean warming but is resilient to ocean acidification in our experiments. Microbial taxa differed in relative abundance with temperature, implying different adaptive strategies and ecological specializations among microorganisms. Additionally, a small proportion (~0.2% of the total taxa) of the relatively abundant microbial taxa were core constituents (>50% occurrence among samples) across different temperatures, p CO 2 levels, or time. Some taxa, including A4b bacteria and members of the family Saprospiraceae in the phyla Chloroflexi (syn. Chloroflexota ) and Bacteroidetes (syn. Bacteroidota ), respectively, as well as protists in the genera Labyrinthula and Aplanochytrium in the class Labyrinthulomycetes , and Pseudoperkinsus tapetis in the class Ichthyosporea were core constituents across temperatures, p CO 2 levels, and time, suggesting that they play an important, albeit unknown, role in maintaining the structural and functional stability of the Pacific oyster spat microbiome in response to ocean warming and acidification. These findings highlight the flexibility of the spat microbiome to environmental changes. IMPORTANCE Pacific oysters are the most economically important and widely farmed species of oyster, and their production depends on healthy oyster spat. In turn, spat health and productivity are affected by the associated microbiota; yet, studies have not scrutinized the effects of temperature and p CO 2 on the prokaryotic and eukaryotic microbiomes of spat. Here, we show that both the prokaryotic and, for the first time, eukaryotic microbiome of Pacific oyster spat are surprisingly resilient to changes in acidification, but sensitive to ocean warming. The findings have potential implications for oyster survival amid climate change and underscore the need to understand temperature and p CO 2 effects on the microbiome and the cascading effects on oyster health and productivity.

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Review of the protist Labyrinhula spp. and its relationship to seagrass disease under the influence of anthropogenic activities

Wang,

Yu,

et al. 2024

Front. Microbiol.

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Anthropogenic activities are driving significant changes in coastal ecological environments, increasingly spotlighting microorganisms associated with seagrass bed ecosystems. Labyrinthula is primarily recognized as a saprophytic protist associated with marine detritus, and it also acts as an opportunistic pathogen affecting marine algae, terrestrial plants and mollusks, especially in coastal environments. The genus plays a key role in the decomposition of marine detritus, facilitated by its interactions with diatoms and through the utilization of a diverse array of carbohydrate-active enzymes to decompose seagrass cell walls. However, human activities have significantly influenced the prevalence and severity of seagrass wasting disease (SWD) through factors such as climate warming, increased salinity and ocean acidification. The rise in temperature and salinity, exacerbated by human-induced climate change, has been shown to increase the susceptibility of seagrass to Labyrinthula, highlighting the adaptability of pathogen to environmental stressors. Moreover, the role of seagrass in regulating pathogen load and their immune response to Labyrinthula underscore the complex dynamics within these marine ecosystems. Importantly, the genotype diversity of seagrass hosts, environmental stress factors and the presence of marine organisms such as oysters, can influence the interaction mechanisms between seagrass and Labyrinthula. Besides, these organisms have the potential to both mitigate and facilitate pathogen transmission. The complexity of these interactions and their impacts driven by human activities calls for the development of comprehensive multi-factor models to better understand and manage the conservation and restoration of seagrass beds.

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The Prokaryotic and Eukaryotic Microbiome of Pacific Oyster Spat is Shaped by Ocean Warming but not Acidification

Cited by 3 publications

References 117 publications

The core microbiome of cultured Pacific oyster spat develops with age but not mortality

The core microbiome of cultured Pacific oyster spat develops with age but not mortality

The prokaryotic and eukaryotic microbiome of Pacific oyster spat is shaped by ocean warming but not acidification

Review of the protist Labyrinhula spp. and its relationship to seagrass disease under the influence of anthropogenic activities

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