Symbiotic state influences life-history strategy of a clonal cnidarian

Bingham, Brian L.; Dimond, James L.; Muller‐Parker, Gisèle

doi:10.1098/rspb.2014.0548

Cited by 13 publications

(9 citation statements)

References 41 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…We hypothesize that this is corresponding to a stressed state, because higher richness often associates with stress in coral-associated communities; this is thought to be due to a diminishing of microbiome regulation when hosts are stressed (McDevitt-Irwin et al, 2017). This is further supported when previous observations that anemones in the green symbiotic state favor sexual reproduction over asexual reproduction typical of the brown symbiotic state (Bingham et al, 2014), are considered alongside the strong correlation between stress and sexual reproduction in facultative sexual organisms (Ram and Hadany, 2016). Finally, Anthopleura elegantissima only stably associate with Elliptochloris in a narrow range of temperatures and irradiances, suggesting that the symbiosis with Elliptochloris is less favorable (Bates et al, 2010).…”

Section: Elliptochloris-associated Communities Exhibit Higher Richnessupporting

confidence: 66%

“…The paucity of anemones in the green symbiotic state is concordant with experimental evidence that the green algae are less beneficial to A. elegantissima; brown algal symbionts are estimated to contribute about five times as much carbon to their hosts compared to green algal symbionts (Verde and McCloskey, 1996). Furthermore, A. elegantissima, which are facultative sexual reproducing animals, exhibit higher rates of sexual reproduction in the green symbiotic state and higher rates of asexual reproduction in the brown symbiotic state (Bingham et al, 2014). This is in agreement with the common observation that in facultative sexual organisms, sexual reproduction is usually associated with poor conditions (Ram and Hadany, 2016).…”

Section: Introductionsupporting

confidence: 65%

See 1 more Smart Citation

Microbiome Variation in an Intertidal Sea Anemone Across Latitudes and Symbiotic States

et al. 2019

View full text Add to dashboard Cite

Many cnidarians form symbiotic relationships with brown dinoflagellate algae in the genus Symbiodinium. Bacteria are important to this symbiosis, with diverse functions such as providing nutrients to the symbiont and pathogen protection to the cnidarian. Disrupted bacterial communities are associated with thermally stressed cnidarians, which have a higher likelihood of expelling their symbionts, an event called bleaching. To better understand the association between thermal tolerance and bacterial community structure, we studied communities associated with an exceptionally thermal tolerant cnidarian, Anthopleura elegantissima. This intertidal symbiotic sea anemone is distributed from the subtropical waters of Baja California to subarctic Alaska, and experiences daily temperature fluctuations of up to 20 • C. It is also flexible in its symbioses, predominantly hosting Symbiodinium, but occasionally hosting the green algae Elliptochloris marina or existing without symbionts in an aposymbiotic state. We used 16S rRNA gene amplicon sequencing to characterize the natural variation of microbial communities associated with Anthopleura elegantissima in these three symbiotic states and across a latitudinal gradient. In this study, we identified a core microbiome, made up predominantly of low-abundance taxa. We found that the communities associated with A. elegantissima were weakly linked to latitude. Diversity analyses revealed significantly higher species richness values for microbial communities associated with anemones hosting E. marina. Lastly the microbiome communities associated with different symbiotic states were compositionally distinct. Taken together, our results suggest that the structure of microbial communities associated with these temperate cnidarians is tightly linked to symbiotic state and weakly linked to other biogeographic phenomena.

show abstract

Section: Elliptochloris-associated Communities Exhibit Higher Richnessupporting

confidence: 66%

Section: Introductionsupporting

confidence: 65%

Microbiome Variation in an Intertidal Sea Anemone Across Latitudes and Symbiotic States

et al. 2019

View full text Add to dashboard Cite

show abstract

“…Thus, we can conclude that when symbiont density is taken into consideration, S. muscatinei still imposes a greater H 2 O 2 burden on its host. Nonetheless, given that S. muscatinei-bearing anemones exhibit higher fitness than aposymbiotic or E. marina-bearing individuals (Bingham et al 2014), the benefits of hosting S. muscatinei clearly outweigh their costs. These benefits include carbon translocation rates at least 2-3 times higher than for E. marina-bearing anemones under high temperature and irradiance conditions (Engebretson and Muller-Parker 1999, Verde and McCloskey 2001, 2002.…”

Section: Discussionmentioning

confidence: 99%

Photophysiology and hydrogen peroxide generation of the dinoflagellate and chlorophyte symbionts of the sea anemone Anthopleura elegantissima

Dimond

Orechovesky

Oppenheimer

et al. 2017

Journal of Experimental Marine Biology and Ecology

Self Cite

View full text Add to dashboard Cite

Associating with algal symbionts is considered largely beneficial for cnidarians such as corals and sea anemones, yet there are potential costs of hosting symbionts, such as the production of reactive oxygen species. We compared the photophysiology and H 2 O 2 production rates of Symbiodinium muscatinei and Elliptochloris marina, the dinoflagellate and chlorophyte symbionts, respectively, of the temperate sea anemone Anthopleura elegantissima. Analyses of PSII function in the two symbionts, including maximum quantum yield and relative electron transport rates, were consistent with prior studies indicating that E. marina has lower photosynthetic performance than S. muscatinei at high temperature and irradiance. The efficiency of PSII in both symbionts was positively affected by the addition of exogenous catalase, suggesting that both symbionts experience H 2 O 2-mediated declines in PSII efficiency. We found that S. muscatinei produced more H 2 O 2 than E. marina across all treatments, with the highest production under high light and temperature. Results were similar in experiments involving both isolated symbionts and symbionts residing within intact tentacles, indicating that the potential stress of symbiont isolation was not a significant factor biasing our results. Despite the lower typical densities of S. muscatinei relative to E. marina, extrapolations of cell-specific H 2 O 2 production rates to the intact symbiosis suggest that S. muscatinei imposes a greater H 2 O 2 burden on A. elegantissima. Even with this burden, however, the considerably higher productivity and fitness of S. muscatinei-bearing anemones documented in prior studies suggests that the net benefit of hosting S. muscatinei exceeds that of E. marina.

show abstract

“…Intracellular dinoflagellate symbionts provide photosynthetically derived nutrients and thus metabolic support to their cnidarian hosts (Bergschneider and Muller-Parker 2008 ). These nutrients presumably facilitate host sexual function, as gonad development is constrained by symbiont loss in corals (Szmant and Gassman 1990 ; Michalek-Wagner and Willis 2001a , 2001b ; Bingham et al 2014 ). However, the effects of symbiont loss on reproductive function in actiniarians have not been well studied.…”

Section: Discussionmentioning

confidence: 99%

Body size and symbiotic status influence gonad development in Aiptasia pallida anemones

2016

View full text Add to dashboard Cite

Pale anemones (Aiptasia pallida) coexist with dinoflagellates (primarily Symbiodinium minutum) in a mutualistic relationship. The purpose of this study was to investigate the role of these symbionts in gonad development of anemone hosts. Symbiotic and aposymbiotic anemones were subjected to light cycles that induced gametogenesis. These anemones were then sampled weekly for nine weeks, and gonad development was analyzed histologically. Anemone size was measured as mean body column diameter, and oocytes or sperm follicles were counted for each anemone. Generalized linear models were used to evaluate the influence of body size and symbiotic status on whether gonads were present and on the number of oocytes or sperm follicles produced. Body size predicted whether gonads were present, with larger anemones being more likely than smaller anemones to develop gonads. Both body size and symbiotic status predicted gonad size, such that larger and symbiotic anemones produced more oocytes and sperm follicles than smaller and aposymbiotic anemones. Overall, only 22 % of aposymbiotic females produced oocytes, whereas 63 % of symbiotic females produced oocytes. Similarly, 6 % of aposymbiotic males produced sperm follicles, whereas 60 % of symbiotic males produced sperm follicles. Thus, while gonads were present in 62 % of symbiotic anemones, they were present in only 11 % of aposymbiotic anemones. These results indicate that dinoflagellate symbionts influence gonad development and thus sexual maturation in both female and male Aiptasia pallida anemones. This finding substantiates and expands our current understanding of the importance of symbionts in the development and physiology of cnidarian hosts.Electronic supplementary materialThe online version of this article (doi:10.1007/s13199-016-0456-1) contains supplementary material, which is available to authorized users.

show abstract

Symbiotic state influences life-history strategy of a clonal cnidarian

Cited by 13 publications

References 41 publications

Microbiome Variation in an Intertidal Sea Anemone Across Latitudes and Symbiotic States

Microbiome Variation in an Intertidal Sea Anemone Across Latitudes and Symbiotic States

Photophysiology and hydrogen peroxide generation of the dinoflagellate and chlorophyte symbionts of the sea anemone Anthopleura elegantissima

Body size and symbiotic status influence gonad development in Aiptasia pallida anemones

Contact Info

Product

Resources

About