Variation in symbiont uptake in the early ontogeny of the upside-down jellyfish, Cassiopea spp.

Mellas, Rachel E.; McIlroy, Shelby E.; Fitt, William K.; Coffroth, Mary Alice

doi:10.1016/j.jembe.2014.04.026

Cited by 41 publications

(42 citation statements)

References 38 publications

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“…Hosting multiple variants of Symbiodinium may confer a fitness benefit to the host, particularly if the composition of the symbiont community varies (e.g., via competitive displacement) in response to changing environmental conditions (so‐called symbiont shuffling) (Berkelmans & Van Oppen, ; Little, Van Oppen, & Willis, ). However, in our study, we only detected Symbiodinium ITS2 type C1, which is a generalist symbiont (Lajeunesse, ) that has been observed in >100 host species, including Cassiopea (Franklin, Stat, Pochon, Putnam, & Gates, ; Mellas, Mcilroy, Fitt, & Coffroth, ; Tonk, Bongaerts, Sampayo, & Hoegh‐Guldberg, ). As we detected only one variant of Symbiodinium , there was no evidence of major symbiont shuffling of the dominant symbiont populations, although we cannot rule out that the techniques used in this study and the ITS2 marker may not fully capture changes in dominance of population heterogeneity, notably for type C1 (see Howells, Willis, Bay, & Van Oppen, ; Wham & Lajeunesse, ).…”

Section: Discussionmentioning

confidence: 61%

“…populations in Australia are at present unknown, it is well demonstrated that Cassiopea spp. polyps can host multiple variants of Symbiodinium and acquire additional symbiont types at the polyp stage (including clades A, B, C and D; Mellas et al., ). However, polyps in our experiment were not exposed to exogenous Symbiodinium cells and thus could not have acquired new symbiont types unless symbionts were shared horizontally between polyps (see Sachs & Wilcox, ).…”

Section: Discussionmentioning

confidence: 99%

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Symbiodinium mitigate the combined effects of hypoxia and acidification on a noncalcifying cnidarian

Klein

Pitt

Nitschke

et al. 2017

Global Change Biology

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Anthropogenic nutrient inputs enhance microbial respiration within many coastal ecosystems, driving concurrent hypoxia and acidification. During photosynthesis, Symbiodinium spp., the microalgal endosymbionts of cnidarians and other marine phyla, produce O and assimilate CO and thus potentially mitigate the exposure of the host to these stresses. However, such a role for Symbiodinium remains untested for noncalcifying cnidarians. We therefore contrasted the fitness of symbiotic and aposymbiotic polyps of a model host jellyfish (Cassiopea sp.) under reduced O (~2.09 mg/L) and pH (~ 7.63) scenarios in a full-factorial experiment. Host fitness was characterized as asexual reproduction and their ability to regulate internal pH and Symbiodinium performance characterized by maximum photochemical efficiency, chla content and cell density. Acidification alone resulted in 58% more asexual reproduction of symbiotic polyps than aposymbiotic polyps (and enhanced Symbiodinium cell density) suggesting Cassiopea sp. fitness was enhanced by CO -stimulated Symbiodinium photosynthetic activity. Indeed, greater CO drawdown (elevated pH) was observed within host tissues of symbiotic polyps under acidification regardless of O conditions. Hypoxia alone produced 22% fewer polyps than ambient conditions regardless of acidification and symbiont status, suggesting Symbiodinium photosynthetic activity did not mitigate its effects. Combined hypoxia and acidification, however, produced similar numbers of symbiotic polyps compared with aposymbiotic kept under ambient conditions, demonstrating that the presence of Symbiodinium was key for mitigating the combined effects of hypoxia and acidification on asexual reproduction. We hypothesize that this mitigation occurred because of reduced photorespiration under elevated CO conditions where increased net O production ameliorates oxygen debt. We show that Symbiodinium play an important role in facilitating enhanced fitness of Cassiopea sp. polyps, and perhaps also other noncalcifying cnidarian hosts, to the ubiquitous effects of ocean acidification. Importantly we highlight that symbiotic, noncalcifying cnidarians may be particularly advantaged in productive coastal waters that are subject to simultaneous hypoxia and acidification.

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Section: Discussionmentioning

confidence: 61%

Section: Discussionmentioning

confidence: 99%

Symbiodinium mitigate the combined effects of hypoxia and acidification on a noncalcifying cnidarian

Klein

Pitt

Nitschke

et al. 2017

Global Change Biology

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“…Species within the ITS2‐type B1 group dominate 1‐ to 2‐year‐old B. asbestinum juveniles (Poland et al, ); the B. minutum culture used in this study has been found in newly settled field recruits, but it is a distinct genotype from that which eventually dominates in juveniles in nature. S. microadriaticum and D. trenchii are both common constituents of Caribbean cnidarian–dinoflagellate associations (LaJeunesse, Parkinson, & Reimer, ; Mellas, McIlroy, Fitt, & Coffroth, ; Thornhill, LaJeunesse, Kemp, Fitt, & Schmidt, ) and have been found in newly settled B. asbestinum in the field (Coffroth et al, ; Poland et al, ).…”

Section: Methodsmentioning

confidence: 99%

Competition and succession among coral endosymbionts

McIlroy

Cunning

Baker

et al. 2019

Ecology and Evolution

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Host species often support a genetically diverse guild of symbionts, the identity and performance of which can determine holobiont fitness under particular environmental conditions. These symbiont communities are structured by a complex set of potential interactions, both positive and negative, between the host and symbionts and among symbionts. In reef‐building corals, stable associations with specific symbiont species are common, and we hypothesize that this is partly due to ecological mechanisms, such as succession and competition, which drive patterns of symbiont winnowing in the initial colonization of new generations of coral recruits. We tested this hypothesis using the experimental framework of the de Wit replacement series and found that competitive interactions occurred among symbionts which were characterized by unique ecological strategies. Aposymbiotic octocoral recruits within high‐ and low‐light environments were inoculated with one of three Symbiodiniaceae species as monocultures or with cross‐paired mixtures, and we tracked symbiont uptake using quantitative genetic assays. Priority effects, in which early colonizers excluded competitive dominants, were evidenced under low light, but these early opportunistic species were later succeeded by competitive dominants. Under high light, a more consistent competitive hierarchy was established in which competitive dominants outgrew and limited the abundance of others. These findings provide insight into mechanisms of microbial community organization and symbiosis breakdown and recovery. Furthermore, transitions in competitive outcomes across spatial and temporal environmental variation may improve lifetime host fitness.

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“…106 Table 5.2 The significant comparisons of the Kaplan-Meier curves for the symbiont acquisition of Isopora palifera. pedunculatus (Davy et al 1997) and Aiptasia pulchella (Davy and Cook 2001); a great diversity of octocorals (Van Oppen et al 2005); and jellyfish (Mellas et al 2014). The most striking and well-studied of these are the endosymbioses of unicellular microalgae and scleractinian corals, where the exchange of the products of algal photosynthesis and nitrogenous animal waste ultimately forms the nutritional basis of coral reefs (Muscatine et al 1981;Voolstra et al 2009).…”

Section: List Of Tablesmentioning

confidence: 99%

“…Many host species, including jellyfish of the Cassiopea genus (Mellas et al 2014) and 80-85% of all scleractinian coral species (Richmond and Hunter 1990;Baird et al 2009) initially lack symbionts (i.e.…”

Section: Introductionmentioning

confidence: 99%

The free-living Symbiodinium reservoir and scleractinian coral symbiont acquisition

Nitschke¹

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The genus Symbiodinium (Dinophyceae, Suessiales), a group of geographically widespread marine dinoflagellates, comprises numerous ecologically and genetically distinct taxa. Symbiodinium spp.establish intracellular symbioses with cnidarians, infecting hosts such as jellyfish, sea anemones, octocorals and reef-building corals. The energetic demands of hosts can be met at varying levels by Symbiodinium through translocation of photosynthetically-fixed carbon, assisting in the formation of coral reefs. The cnidarian-dinoflagellate symbiosis is relatively well studied. In contrast, empirical data for population dynamics, distribution, and physiology of free-living Symbiodinium are limited.Therefore this thesis aims to characterise the dynamics between free-living Symbiodinium cells, hosts, and their habitat.Free-living Symbiodinium cells have been identified in reef sediment, and this study investigated whether adult coral colonies are a significant source of benthic Symbiodinium cells. Acropora millepora colonies were translocated to bare patches of sediment (Heron Reef, Great Barrier Reef, Australia), and the surrounding sediment was sampled for Symbiodinium cells over a period of 18 months. An 8-fold increase in visually-identified cells relative to the background population was recorded from the sediment at the immediate base of coral colonies. Symbiodinium abundance returned to background levels after the removal of the coral. These fine-scale changes in the distribution of cells suggests that hard-coral may be an important 'passive' source of Symbiodinium.The 'active' supply of Symbiodinium cells to the benthos was investigated through direct contact of coral tissue with sediment. Symbiont loss was induced in the coral Pocillopora damicornis through burial of coral branches. Peak cell abundance in the sediment occurred after four days, but the photophysiology (F v /F m ) of the Symbiodinium cells was significantly impaired. By day 12, Symbiodinium cells were present only in low concentrations in sediment samples, and the majority of cells were substantially degraded. In this study, Symbiodinium appeared to survive only transiently following expulsion, with an approximate window of viability of seven days. Such a period may be sufficient for coral recruits to make contact with potential symbionts in situ.Elevated temperatures induce a range of serious, deleterious effects in Symbiodinium. The potential amelioration of these effects was investigated, testing the hypothesis that Symbiodinium cells find refuge from stress when cultured within sediment. An exclusively free-living clade A (not known to form symbioses) and the symbiosis-forming type A1 were grown with or without a microhabitat of carbonate sediment at 25°C, 28°C or 31°C. The exclusively free-living clade A was physiologically superior to symbiosis-forming A1 across all measured variables and treatment combinations: it iii reproduced faster within the sediment, exhibited high levels of motility and maintained a stable maximum quantum yield (F ...

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Variation in symbiont uptake in the early ontogeny of the upside-down jellyfish, Cassiopea spp.

Cited by 41 publications

References 38 publications

Symbiodinium mitigate the combined effects of hypoxia and acidification on a noncalcifying cnidarian

Symbiodinium mitigate the combined effects of hypoxia and acidification on a noncalcifying cnidarian

Competition and succession among coral endosymbionts

The free-living Symbiodinium reservoir and scleractinian coral symbiont acquisition

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