Assessing the chronic toxicity of copper and aluminium to the tropical sea anemone Exaiptasia pallida

Exaiptasia diaphana, a tropical sea anemone known as Aiptasia, is a tractable model system for studying the cellular, physiological, and ecological characteristics of cnidarian-dinoflagellate symbiosis. Aiptasia is widely used as a proxy for coral-algal symbiosis, since both Aiptasia and corals form a symbiosis with members of the family Symbiodiniaceae. Laboratory strains of Aiptasia can be maintained in both the symbiotic (Sym) and aposymbiotic (Apo, without algae) states. Apo Aiptasia allow for the study of the influence of symbiosis on different biological processes and how different environmental conditions impact symbiosis. A key feature of Aiptasia is the ease of propagating both Sym and Apo individuals in the laboratory through a process called pedal laceration. In this form of asexual reproduction, small pieces of tissue rip away from the pedal disc of a polyp, then these lacerates eventually develop tentacles and grow into new polyps. While pedal laceration has been described in the past, details of how tentacles are formed or how symbiotic and nutritional state influence this process are lacking. Here we describe the stages of development in both Sym and Apo pedal lacerates. Our results show that Apo lacerates develop tentacles earlier than Sym lacerates, while over the course of 20 days, Sym lacerates end up with a greater number of tentacles. We describe both tentacle and mesentery patterning during lacerate development and show that they form through a single pattern in early stages regardless of symbiotic state. In later stages of development, Apo lacerate tentacles and mesenteries progress through a single pattern, while variable patterns were observed in Sym lacerates. We discuss how Aiptasia lacerate mesentery and tentacle patterning differs from oral disc regeneration and how these patterning events compare to postembryonic development in Nematostella vectensis, another widely-used sea anemone model. In addition, we demonstrate that Apo lacerates supplemented with a putative nutrient source developed an intermediate number of tentacles between un-fed Apo and Sym lacerates. Based on these observations, we hypothesize that pedal lacerates progress through two different, putatively nutrient-dependent phases of development. In the early phase, the lacerate, regardless of symbiotic state, preferentially uses or relies on nutrients carried over from the adult polyp. These resources are sufficient for lacerates to develop into a functional polyp. In the late phase of development, continued growth and tentacle formation is supported by nutrients obtained from either symbionts and/or the environment through heterotrophic feeding. Finally, we advocate for the implementation of pedal lacerates as an additional resource in the Aiptasia model system toolkit for studies of cnidarian-dinoflagellate symbiosis.

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Cellular mechanisms underlying temperature-induced bleaching in the tropical sea anemone Aiptasia pulchella

Journal of Experimental Biology ◽

10.1242/jeb.204.20.3443 ◽

2001 ◽

Vol 204 (20) ◽

pp. 3443-3456 ◽

Cited By ~ 3

Author(s):

Sara J. Sawyer ◽

Leonard Muscatine

Keyword(s):

Protein Phosphorylation ◽

Plasma Membranes ◽

Sea Anemone ◽

Host Cells ◽

Pocillopora Damicornis ◽

Cellular Mechanisms ◽

Paramagnetic Resonance ◽

Aiptasia Pulchella ◽

Tropical Sea ◽

And Control

SUMMARY Temperature-induced bleaching in symbiotic cnidarians is a result of the detachment and loss of host cells containing symbiotic algae. We tested the hypothesis that host cell detachment is evoked through a membrane thermotropic event causing an increase in intracellular calcium concentration, [Ca2+]i, which could then cause collapse of the cytoskeleton and perturb cell adhesion. Electron paramagnetic resonance measurements of plasma membranes from the tropical sea anemone Aiptasia pulchella and the Hawaiian coral Pocillopora damicornis labeled with 2,2,6,6-tetramethylpiperidine-1-oxyl (TEMPO) revealed no membrane thermotropic event. In addition, intracellular imaging using Fura-2AM as well as labeling anemones with 45Ca revealed no significant change in [Ca2+]i. However, bleaching could be evoked at ambient temperature with 25 mmol l–1 caffeine without affecting [Ca2+]i. [Ca2+]i could be altered with ionomycin in isolated host cells, but ionomycin could not induce bleaching in A. pulchella. As caffeine can affect levels of intracellular protein phosphorylation, the ability of other agents that alter intracellular levels of protein phosphorylation to evoke bleaching was investigated. The protein phosphatase inhibitor vanadate could induce bleaching in A. pulchella. Two-dimensional gels of 32P-labeled proteins from cold-shocked, caffeine-treated and control anemones show that both temperature shock and caffeine alter the array of phosphorylated host soluble proteins. We conclude that cnidarian bleaching is linked to a temperature-induced alteration in protein phosphorylation.

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Experimentally Induced Bleaching in the Sea Anemone Exaiptasia Supports Glucose as a Main Metabolite Associated with Its Symbiosis

Journal of Marine Biology ◽

10.1155/2017/3130723 ◽

2017 ◽

Vol 2017 ◽

pp. 1-7 ◽

Cited By ~ 4

Author(s):

Víctor Hugo Molina ◽

Raúl Eduardo Castillo-Medina ◽

Patricia Elena Thomé

Keyword(s):

Calcium Carbonate ◽

Sea Anemone ◽

Main Metabolite ◽

Glucose Levels ◽

Carbon Translocation ◽

Specific Activities ◽

Glycerol 3 Phosphate Dehydrogenase ◽

Glucose 6 Phosphate Dehydrogenase ◽

Exaiptasia Pallida ◽

Photosynthate Translocation

Our current understanding of carbon exchange between partners in the Symbiodinium-cnidarian symbioses is still limited, even though studies employing carbon isotopes have made us aware of the metabolic complexity of this exchange. We examined glycerol and glucose metabolism to better understand how photosynthates are exchanged between host and symbiont. The levels of these metabolites were compared between symbiotic and bleached Exaiptasia pallida anemones, assaying enzymes directly involved in their metabolism. We measured a significant decrease of glucose levels in bleached animals but a significant increase in glycerol and G3P pools, suggesting that bleached animals degrade lipids to compensate for the loss of symbionts and seem to rely on symbiotic glucose. The lower glycerol 3-phosphate dehydrogenase but higher glucose 6-phosphate dehydrogenase specific activities measured in bleached animals agree with a metabolic deficit mainly due to the loss of glucose from the ruptured symbiosis. These results corroborate previous observations on carbon translocation from symbiont to host in the sea anemone Exaiptasia, where glucose was proposed as a main translocated metabolite. To better understand photosynthate translocation and its regulation, additional research with other symbiotic cnidarians is needed, in particular, those with calcium carbonate skeletons.

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Responses of the sea anemone, Exaiptasia pallida , to ocean acidification conditions and zinc or nickel exposure

Aquatic Toxicology ◽

10.1016/j.aquatox.2016.11.014 ◽

2017 ◽

Vol 182 ◽

pp. 120-128 ◽

Cited By ~ 10

Author(s):

Christina G. Duckworth ◽

Codie R. Picariello ◽

Rachel K. Thomason ◽

Krina S. Patel ◽

Gretchen K. Bielmyer-Fraser

Keyword(s):

Ocean Acidification ◽

Sea Anemone ◽

Nickel Exposure ◽

Exaiptasia Pallida

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Worldwide exploration of the microbiome harbored by the cnidarian model, Exaiptasia pallida indicates a lack of bacterial association specificity at a lower taxonomic rank

10.7287/peerj.preprints.2338v1 ◽

2016 ◽

Author(s):

Tanya Brown ◽

Christopher Otero ◽

Alejandro Grajales ◽

Estefania Rodriguez ◽

Mauricio Rodriguez-Lanetty

Keyword(s):

Community Structure ◽

Microbial Community ◽

Bacterial Community ◽

Bacterial Species ◽

Sea Anemone ◽

Microbial Consortia ◽

Rrna Gene ◽

Core Microbiome ◽

Wide Range ◽

Exaiptasia Pallida

Examination of host-microbe interactions in basal metazoans, such as cnidarians is of great interest from an evolutionary perspective to understand how host-microbial consortia have evolved. To address this problem, we analyzed whether the bacterial community associated with the cosmopolitan and model sea anemone Exaiptasia pallida shows specific patterns across worldwide populations ranging from the Caribbean Sea, and the Atlantic and Pacific oceans. By comparing sequences of the V1-V4 hypervariable regions of the bacterial 16S rRNA gene, we revealed that anemones host a complex and diverse microbial community. When examined at the phylum level, bacterial diversity and abundance associated with E. pallida are broadly conserved across geographic space with samples, containing largely Proteobacteria and Bacteroides. However, the species-level makeup within these phyla differs drastically across space suggesting a high-level core microbiome with local adaptation of the constituents. Indeed, no bacterial OTU was ubiquitously found in all anemones samples. We also revealed changes in the microbial community structure after rearing anemone specimens in captivity within a period of four months. These results contrast with the postulation that cnidarian hosts might actively select and maintain species-specific microbial communities that could have resulted from an intimate co-evolution process. Instead, our findings suggest that environmental settings, not host specificity seem to dictate bacterial community structure associated with this sea anemone. More than maintaining a specific composition of bacterial species some cnidarians associate with a wide range of bacterial species as long as they provide the same physiological benefits towards the maintenance of a healthy host. The examination of the previously uncharacterized bacterial community associated with the cnidarian sea anemone model E. pallida is the first global-scale study of its kind.

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Worldwide exploration of the microbiome harbored by the cnidarian model,Exaiptasia pallida(Agassiz in Verrill, 1864) indicates a lack of bacterial association specificity at a lower taxonomic rank

PeerJ ◽

10.7717/peerj.3235 ◽

2017 ◽

Vol 5 ◽

pp. e3235 ◽

Cited By ~ 8

Author(s):

Tanya Brown ◽

Christopher Otero ◽

Alejandro Grajales ◽

Estefania Rodriguez ◽

Mauricio Rodriguez-Lanetty

Keyword(s):

Community Structure ◽

Microbial Community ◽

Bacterial Community ◽

Bacterial Species ◽

Sea Anemone ◽

Microbial Consortia ◽

Rrna Gene ◽

Core Microbiome ◽

Wide Range ◽

Exaiptasia Pallida

Examination of host-microbe interactions in early diverging metazoans, such as cnidarians, is of great interest from an evolutionary perspective to understand how host-microbial consortia have evolved. To address this problem, we analyzed whether the bacterial community associated with the cosmopolitan and model sea anemoneExaiptasia pallidashows specific patterns across worldwide populations ranging from the Caribbean Sea, and the Atlantic and Pacific oceans. By comparing sequences of the V1–V3 hypervariable regions of the bacterial 16S rRNA gene, we revealed that anemones host a complex and diverse microbial community. When examined at the phylum level, bacterial diversity and abundance associated withE. pallidaare broadly conserved across geographic space with samples, containing largelyProteobacteriaandBacteroides.However, the species-level makeup within these phyla differs drastically across space suggesting a high-level core microbiome with local adaptation of the constituents. Indeed, no bacterial OTU was ubiquitously found in all anemones samples. We also revealed changes in the microbial community structure after rearing anemone specimens in captivity within a period of four months. Furthermore, the variation in bacterial community assemblages across geographical locations did not correlate with the composition of microalgalSymbiodiniumsymbionts. Our findings contrast with the postulation that cnidarian hosts might actively select and maintain species-specific microbial communities that could have resulted from an intimate co-evolution process. The fact thatE. pallidais likely an introduced species in most sampled localities suggests that this microbial turnover is a relatively rapid process. Our findings suggest that environmental settings, not host specificity, seem to dictate bacterial community structure associated with this sea anemone. More than maintaining a specific composition of bacterial species some cnidarians associate with a wide range of bacterial species as long as they provide the same physiological benefits towards the maintenance of a healthy host. The examination of the previously uncharacterized bacterial community associated with the cnidarian sea anemone modelE. pallidais the first global-scale study of its kind.

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