Every refuge has its price: Ostreobium as a model for understanding how algae can live in rock and stay in business

Tandon, Kshitij; Pasella, Marisa M.; Iha, Cíntia; Ricci, Francesco; Hu, Juntong; O’Kelly, Charles J.; Medina, Mónica; Kühl, Michael; Verbruggen, Heroen

doi:10.1016/j.semcdb.2022.03.010

Cited by 17 publications

(11 citation statements)

References 88 publications

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“…Considering other chemical species (inorganic and organic carbon, various acid/base couples) and reactions in our model would enable the representation of calcification and carbon transfer between symbionts and host, and such work is in progress. Another desired expansion could be a more detailed account of metabolic processes in the coral skeleton, performed by the endolithic algae and microbes (Ricci et al, 2019; Tandon et al, 2022).…”

Section: Resultsmentioning

confidence: 99%

Modeling the radiative, thermal and chemical microenvironment of 3D scanned corals

Murthy

Picioreanu

Kühl

2023

Preprint

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1: Reef building corals are efficient biological collectors of solar radiation and consist of a thin stratified tissue layer spread over a light scattering calcium carbonate skeleton surface that together construct complex three dimensional (3D) colony structures forming the foundation of coral reefs. They exhibit a vast diversity of structural forms to maximize photosynthesis of their dinoflagellate endosymbionts (Symbiodiniaceae), while simultaneously minimizing photodamage. The symbiosis takes place in the presence of dynamic gradients of light, temperature and chemical species that are affected by the interaction of incident irradiance and water flow with the coral colony. 2: We developed a multiphysics modelling approach to simulate microscale spatial distribution of light, temperature and O2 in coral fragments with accurate morphology determined by 3D scanning techniques. 3: Model results compared well with spatial measurements of light, O2 and temperature under similar flow and light conditions. The model enabled us to infer the effect of coral morphology and light scattering in tissue and skeleton on the internal light environment experienced by the endosymbionts, as well as the combined contribution of light, water flow and ciliary movement on O2 and temperature distributions in the coral. 4: The multiphysics modeling approach is general enough to enable simulation of external and internal light, O2 and temperature microenvironments in 3D scanned coral species with varying degrees of branching and morphology under different environmental conditions. This approach is also relevant for simulating structure-function relationships in other benthic systems such as photosynthetic biofilms and aquatic plant tissue, and can also be adapted to other sessile organisms such as symbiont-bearing giant clams, ascidians, jellyfish or foraminifera. The model could also be useful in more applied research such as optimization of 3D bioprinted constructs where different designs can be evaluated and optimized.

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Section: Resultsmentioning

confidence: 99%

Modeling the radiative, thermal and chemical microenvironment of 3D scanned corals

Murthy

Picioreanu

Kühl

2023

Preprint

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“…The calcium carbonate (CaCO 3 ) matrix of the skeleton of living scleractinian corals is colonized by endolithic communities of eukaryotes and prokaryotes (Marcelino et al, 2017; Marcelino & Verbruggen, 2016; Pollock et al, 2018; Ricci et al, 2022; Tandon, Ricci, et al, 2022). Endolithic, coenocytic green algae in the genus Ostreobium are among the most conspicuous eukaryotes found in this environment (Del Campo et al, 2017; Iha et al, 2021; Marcelino & Verbruggen, 2016; Ricci et al, 2021; Tandon, Pasella, et al, 2022), and they often form a distinct green band positioned one to a few millimetres below the coral tissue. The ability of Ostreobium filaments to dissolve and drill into the CaCO 3 matrix makes them ubiquitous colonizers of the coral skeleton (Ralph et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

Fine‐scale mapping of physicochemical and microbial landscapes of the coral skeleton

Ricci

Tandon

Moßhammer

et al. 2023

Environmental Microbiology

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The coral skeleton harbours a diverse community of bacteria and microeukaryotes exposed to light, O2 and pH gradients, but how such physicochemical gradients affect the coral skeleton microbiome remains unclear. In this study, we employed chemical imaging of O2 and pH, hyperspectral reflectance imaging and spatially resolved taxonomic and inferred functional microbiome characterization to explore links between the skeleton microenvironment and microbiome in the reef‐building corals Porites lutea and Paragoniastrea benhami. The physicochemical environment was more stable in the deep skeleton, and the diversity and evenness of the bacterial community increased with skeletal depth, suggesting that the microbiome was stratified along the physicochemical gradients. The bulk of the coral skeleton was in a low O2 habitat, whereas pH varied from pH 6–9 with depth. Physicochemical gradients of O2 and pH of the coral skeleton explained the β‐diversity of the bacterial communities, and skeletal layers that showed O2 peaks had a higher relative abundance of endolithic algae, reflecting a link between the abiotic environment and the microbiome composition. Our study links the physicochemical, microbial and functional landscapes of the coral skeleton and provides new insights into the involvement of skeletal microbes in the coral holobiont metabolism.

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“…Here, the diversity of Ostreobium -associated bacteria was investigated in two distinct lineages, each exposed to three distinct salinity levels. Experiments were conducted on two genotyped strain representatives of rbc L clade P1 (010) and rbc L clade P14 (06) lineages sensu Massé et al ., 2020, which both belong to Ostreobium lineage 3 sensu Tandon et al ., 2022, within the Ostreobineae suborder. The culture medium salinity was manipulated in order to investigate Ostreobium tolerance to salinity increase and related changes in its associated bacteria, in multiple cultures of each strain, long-term acclimatized (9-13 months) to ecologically relevant low (32.9 psu), medium (35.1 psu) and high salinities (40.2 psu).…”

Section: Introductionmentioning

confidence: 99%

Bacterial microbiota ofOstreobium, the coral-isolated chlorophyte ectosymbiont, at contrasted salinities

Massé¹,

Detang²,

Duval³

et al. 2023

Preprint

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Microscopic filaments of the siphonous green algae Ostreobium (Ulvophyceae, Bryopsidales) colonize and dissolve the calcium carbonate skeletons of coral colonies, in shallow-water reef environments of contrasted salinities. Their bacterial composition and plasticity in response to salinity remain unknown. Here, we analyzed the bacteria associated with coral-isolated Ostreobium strains from two distinct rbcL lineages, representative of IndoPacific environmental phylotypes, that had been pre-acclimatized (>9months) to three ecologically-relevant reef salinities: 32.9, 35.1 and 40.2 psu. Bacterial phylotypes were visualized at filament scale by CARD-FISH in algal tissue sections, localized to the surface, within filaments or in the algal mucilage. Ostreobium-associated communities, characterized by bacterial 16S rRNA metabarcoding of cultured thalli and corresponding supernatants, were structured by host genotype more than salinity and partly overlapped with those of environmental (Ostreobium-colonized) coral skeletons. Alphaproteobacteria dominated the thalli communities, enriched in Kiloniellaceae or Rhodospirillaceae depending on algal genotype. A small core microbiota composed of 7 ASVs (~1.5% of thalli ASVs, 19%-36% cumulated proportions), shared by multiple cultures of both Ostreobium genotypes and persistent across 3 salinities, included putative intracellular Amoebophilus and Rickettsiales bacteria. This novel knowledge on the taxonomic diversity of Ostreobium bacterial associates paves the way to functional interaction studies within the coral holobiont.

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Every refuge has its price: Ostreobium as a model for understanding how algae can live in rock and stay in business

Cited by 17 publications

References 88 publications

Modeling the radiative, thermal and chemical microenvironment of 3D scanned corals

Modeling the radiative, thermal and chemical microenvironment of 3D scanned corals

Fine‐scale mapping of physicochemical and microbial landscapes of the coral skeleton

Bacterial microbiota ofOstreobium, the coral-isolated chlorophyte ectosymbiont, at contrasted salinities

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