Evolution of symbiosis in hermatypic corals: A model of the past, present, and future

Antonelli, P. L.; Rutz, Solange F.; Sammarco, Paul W.; Strychar, Kevin B.

doi:10.1016/j.nonrwa.2016.05.004

Cited by 6 publications

(7 citation statements)

References 52 publications

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“…Symbiosis is a powerful evolutionary strategy that combines skill sets from separate species to meet environmental challenges (Antonelli, Rutz, Sammarco, & Strychar, 2016). Dinoflagellate symbionts of corals are a classic example of such a partnership.…”

Section: Introductionmentioning

confidence: 99%

Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont Breviolum minutum (Symbiodiniaceae)

Maor-Landaw

Oppen

McFadden

2019

Ecology and Evolution

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Coral-dinoflagellate symbiosis underpins the evolutionary success of corals reefs. Successful exchange of molecules between the cnidarian host and the Symbiodiniaceae algae enables the mutualistic partnership. The algae translocate photosynthate to their host in exchange for nutrients and shelter. The photosynthate must traverse multiple membranes, most likely facilitated by transporters. Here, we compared gene expression profiles of cultured, free-living Breviolum minutum with those of the homologous symbionts freshly isolated from the sea anemone Exaiptasia diaphana, a widely used model for coral hosts. Additionally, we assessed expression levels of a list of candidate host transporters of interest in anemones with and without symbionts. Our transcriptome analyses highlight the distinctive nature of the two algal life stages, with many gene expression level changes correlating to the different morphologies, cell cycles, and metabolisms adopted in hospite versus free-living.Morphogenesis-related genes that likely underpin the metamorphosis process observed when symbionts enter a host cell were up-regulated. Conversely, many downregulated genes appear to be indicative of the protective and confined nature of the symbiosome. Our results emphasize the significance of transmembrane transport to the symbiosis, and in particular of ammonium and sugar transport. Further, we pinpoint and characterize candidate transporters-predicted to be localized variously to the algal plasma membrane, the host plasma membrane, and the symbiosome membrane-that likely serve pivotal roles in the interchange of material during symbiosis.Our study provides new insights that expand our understanding of the molecular exchanges that underpin the cnidarian-algal symbiotic relationship. K E Y W O R D S Breviolum minutum, Exaiptasia diaphana, free-living, in hospite, symbiosis, transporters S U PP O RTI N G I N FO R M ATI O N Additional supporting information may be found online in the Supporting Information section. How to cite this article: Maor-Landaw K, van Oppen MJH, McFadden GI. Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont Breviolum minutum (Symbiodiniaceae).

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Section: Introductionmentioning

confidence: 99%

Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont Breviolum minutum (Symbiodiniaceae)

Maor-Landaw

Oppen

McFadden

2019

Ecology and Evolution

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“…This possibility, however, has not yet been functionally confirmed by direct experimentation and the modes of adaptation that are available for a population of holobiont communities have not been investigated in a mathematical framework. Current models of evolutionary change are typically limited to population genetics with a single species of individuals (22) or to ecological (23)(24)(25) and evolutionary game theory models (26) (27) of interactions between free-living or symbiotic (28,29) species. However, these models do not consider the evolution of a holobiont population in which every individual is an interacting community of host and bacteria.…”

Section: Introductionmentioning

confidence: 99%

Darwinian selection of host and bacteria supports emergence of Lamarckian-like adaptation of the system as a whole

Osmanović

Kessler

Rabin

et al. 2016

Preprint

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BackgroundThe relatively fast selection of symbiotic bacteria within hosts and the potential transmission of these bacteria across generations of hosts raise the question of whether interactions between host and bacteria support emergent adaptive capabilities beyond those of germ-free hosts.ResultsTo investigate possibilities for emergent adaptations that may distinguish composite host-microbiome systems from germ-free hosts, we introduce a population genetics model of a host-microbiome system with vertical transmission of bacteria. The host and its bacteria are jointly exposed to a toxic agent, creating a toxic stress that can be alleviated by selection of resistant individuals and by secretion of a detoxification agent (“detox”). We show that toxic exposure in one generation of hosts leads to selection of resistant bacteria, which in turn, increases the toxic tolerance of the host’s offspring. Prolonged exposure to toxin over many host generations promotes additional form of emergent adaptation due to selection of hosts based on detox capabilities of their bacterial community as a whole (as opposed to properties of individual bacteria).ConclusionsThese findings show that interactions between pure Darwinian selections of host and its bacteria can give rise to emergent adaptive capabilities, including Lamarckian-like adaptation of the host-microbiome system.

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“…The symbiosis between algal symbionts and reef-building corals were thought to emerge in the mid-Triassic period ( Stanley, 1981 ). In the ensuing 230 million years of intense differentiation and speciation of the hermatypic corals ( Shepard, 1964 ), the two mutualistic sides, corals and their endosymbiotic algae, have undergone precise coordination or a series of synergistic mutations and formed obligate interdependence ( Antonelli et al, 2016 ). The photosynthetic symbionts have established relatively stable and complex communities in specific coral species and geographic regions ( Lewis et al, 2019 ), and the symbiont biota also changed with the persistence and periodicity of environmental stress ( Lee et al, 2016 ; Lewis et al, 2019 ).…”

Section: Discussionmentioning

confidence: 99%

“…The photosynthetic symbionts have established relatively stable and complex communities in specific coral species and geographic regions ( Lewis et al, 2019 ), and the symbiont biota also changed with the persistence and periodicity of environmental stress ( Lee et al, 2016 ; Lewis et al, 2019 ). On the other hand, adapted to the life in coral cells, symbionts and their host have reached a delicate metabolic balance ( Lin et al, 2019 ) and physiological compromises (such as abandoning sexual reproduction and being compatible with the coral’s immune system) ( Antonelli et al, 2016 ). Therefore, when we attempt to isolate the symbionts from coral cells and establish genetically and physiologically consistent strains, the algae should experience drastic morphological and physiological changes so as to adapt to the new artificial culture environment.…”

Section: Discussionmentioning

confidence: 99%

Monoclonal Culture and Characterization of Symbiodiniaceae C1 Strain From the Scleractinian Coral Galaxea fascicularis

et al. 2021

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The symbiosis between cnidarian hosts and photosynthetic dinoflagellates of the family Symbiodiniaceae (i.e., zooxanthellae) provides the energy foundation of coral reef ecosystems in oligotrophic waters. The structure of symbiont biota and the dominant species of algal symbiont partly shape the environmental adaptability of coral symbiotes. In this study, the algal symbiont cells were isolated from the tentacles of Galaxea fascicularis, a hermatypic coral with obvious differentiation in heat resistance, and were cultured in vitro with an improved L1 medium. An algal monoclonal cell line was established using separated algal culture drops and soft agar plating method, and named by GF19C1 as it was identified as Cladocopium sp. C1 (Symbiodiniaceae) based on its ITS1, ITS2, and the non-coding region of the plastid psbA minicircle (psbAncr) sequences. Most GF19C1 cells were at the coccoid stage of the gymnodinioid, their markedly thickened (ca. two times) cell wall suggests that they developed into vegetative cysts and have sexual and asexual reproductive potential. The average diameter of GF19C1 cells decreased significantly, probably due to the increasing mitotic rate. The chloroplasts volume density of GF19C1 was significantly lower than that of their symbiotic congeners, while the surface area density of thylakoids relative to volumes of chloroplasts was not significantly changed. The volume fraction of vacuoles increased by nearly fivefold, but there was no significant change in mitochondria and accumulation bodies. Light-temperature orthogonal experiments showed that, GF19C1 growth preferred the temperature 25 ± 1°C (at which it is maintained post-isolation) rather than 28 ± 1°C under the light intensity of 42 ± 2 or 62 ± 2 μmol photons m–2 s–1, indicating an inertia for temperature adaptation. The optimum salinity for GF19C1 growth ranged between 28–32 ppt. The monoclonal culture techniques established in this study were critical to clarify the physiological and ecological characteristics of various algal symbiont species, and will be instrumental to further reveal the roles of algal symbionts in the adaptive differentiation of coral-zooxanthellae holobionts in future studies.

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Evolution of symbiosis in hermatypic corals: A model of the past, present, and future

Cited by 6 publications

References 52 publications

Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont Breviolum minutum (Symbiodiniaceae)

Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont Breviolum minutum (Symbiodiniaceae)

Darwinian selection of host and bacteria supports emergence of Lamarckian-like adaptation of the system as a whole

Monoclonal Culture and Characterization of Symbiodiniaceae C1 Strain From the Scleractinian Coral Galaxea fascicularis

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