Photosymbiosis in Marine Pelagic Environments

Not, Fabrice; Probert, Ian; Ribeiro, Catherine Gérikas; Crenn, Klervi; Guillou, Laure; Jeanthon, Christian; Vaulot, Daniel

doi:10.1007/978-3-319-33000-6_11

Cited by 16 publications

(11 citation statements)

References 140 publications

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“…; Not et al . ). Finally, the majority of eukaryotic microalgae have absorbotrophic abilities, but their capacity for uptake of organic carbon vs. non‐carbon elements remains poorly quantified (Flynn et al .…”

Section: Mixotrophy In Aquatic Ecosystemsmentioning

confidence: 97%

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Mixotrophy everywhere on land and in water: thegrand écarthypothesis

2016

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There is increasing awareness that many terrestrial and aquatic organisms are not strictly heterotrophic or autotrophic but rather mixotrophic. Mixotrophy is an intermediate nutritional strategy, merging autotrophy and heterotrophy to acquire organic carbon and/or other elements, mainly N, P or Fe. We show that both terrestrial and aquatic mixotrophs fall into three categories, namely necrotrophic (where autotrophs prey on other organisms), biotrophic (where heterotrophs gain autotrophy by symbiosis) and absorbotrophic (where autotrophs take up environmental organic molecules). Here we discuss their physiological and ecological relevance since mixotrophy is found in virtually every ecosystem and occurs across the whole eukaryotic phylogeny, suggesting an evolutionary pressure towards mixotrophy. Ecosystem dynamics tend to separate light from non-carbon nutrients (N and P resources): the biological pump and water stratification in aquatic ecosystems deplete non-carbon nutrients from the photic zone, while terrestrial plant successions create a canopy layer with light but devoid of non-carbon soil nutrients. In both aquatic and terrestrial environments organisms face a grand ecart (dancer's splits, i.e., the need to reconcile two opposing needs) between optimal conditions for photosynthesis vs. gain of non-carbon elements. We suggest that mixotrophy allows adaptation of organisms to such ubiquist environmental gradients, ultimately explaining why mixotrophic strategies are widespread.

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Section: Mixotrophy In Aquatic Ecosystemsmentioning

confidence: 97%

“…; Not et al . ): indeed, biotrophic mixotrophy, and in particular photosymbioses, are common in oligotrophic environments, where they are assumed to constitute a short cut in the food web (Taylor ; Norris ; Biard et al . ).…”

Section: Mixotrophy In Aquatic Ecosystemsmentioning

confidence: 99%

Mixotrophy everywhere on land and in water: thegrand écarthypothesis

2016

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“…bleaching) (Hallock, ; Hughes et al, ). Many heterotrophic organisms living in oligotrophic waters have evolved obligatory symbioses with photosynthetic microalgae, thus establishing biotrophic mixotrophy (Not et al, ; Selosse, Charpin, & Not, ). This process is called photo‐symbiosis as it makes photosynthesis indirectly available to the host (Selosse et al, ).…”

Section: Introductionmentioning

confidence: 99%

Evolutionary significance of the microbial assemblages of large benthic Foraminifera

Prazeres

Renema

2018

Biological Reviews

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Large benthic Foraminifera (LBF) are major carbonate producers on coral reefs, and are hosts to a diverse symbiotic microbial community. During warm episodes in the geological past, these reef-building organisms expanded their geographical ranges as subtropical and tropical belts moved into higher latitudes. During these range-expansion periods, LBF were the most prolific carbonate producers on reefs, dominating shallow carbonate platforms over reef-building corals. Even though the fossil and modern distributions of groups of species that harbour different types of symbionts are known, the nature, mechanisms, and factors that influence their occurrence remain elusive. Furthermore, the presence of a diverse and persistent bacterial community has only recently gained attention. We examined recent advances in molecular identification of prokaryotic (i.e. bacteria) and eukaryotic (i.e. microalgae) associates, and palaeoecology, and place the partnership with bacteria and algae in the context of climate change. In critically reviewing the available fossil and modern data on symbiosis, we reveal a crucial role of microalgae in the response of LBF to ocean warming, and their capacity to colonise a variety of habitats, across both latitudes and broad depth ranges. Symbiont identity is a key factor enabling LBF to expand their geographic ranges when the sea-surface temperature increases. Our analyses showed that over the past 66 million years (My), diatom-bearing species were dominant in reef environments. The modern record shows that these species display a stable, persistent eukaryotic assemblage across their geographic distribution range, and are less dependent on symbiotic photosynthesis for survival. By contrast, dinoflagellate and chlorophytic species, which show a provincial distribution, tend to have a more flexible eukaryotic community throughout their range. This group is more dependent on their symbionts, and flexibility in their symbiosis is likely to be the driving force behind their evolutionary history, as they form a monophyletic group originating from a rhodophyte-bearing ancestor. The study of bacterial assemblages, while still in its infancy, is a promising field of study. Bacterial communities are likely to be shaped by the local environment, although a core bacterial microbiome is found in species with global distributions. Cryptic speciation is also an important factor that must be taken into consideration. As global warming intensifies, genetic divergence in hosts in addition to the range of flexibility/specificity within host-symbiont associations will be important elements in the continued evolutionary success of LBF species in a wide range of environments. Based on fossil and modern data, we conclude that the microbiome, which includes both algal and bacterial partners, is a key factor influencing the evolution of LBF. As a result, the microbiome assists LBF in colonising a wide range of habitats, and allowed them to become the most important calcifiers on shallow platforms worldwide during perio...

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“…However, the kleptoplasts may (perhaps transiently) benefit from their intracellular presence in the animal host due to enriched availability of carbon dioxide (Serôdio et al, 2014). In metazoans, functional kleptoplasty is taxonomically restricted to Sacoglossa, but it is also found in some protists, including Ciliates and Foraminifera (Pillet, de Vargas & Pawlowski, 2011;Pillet & Pawlowski, 2012;Not et al, 2016). The mechanisms involved in the recognition and incorporation of a symbiont by the animal host are now under intensive investigation.…”

Section: Introductionmentioning

confidence: 99%

Polymorphic adaptations in metazoans to establish and maintain photosymbioses

et al. 2018

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Mutualistic symbioses are common throughout the animal kingdom. Rather unusual is a form of symbiosis, photosymbiosis, where animals are symbiotic with photoautotrophic organisms. Photosymbiosis is found among sponges, cnidarians, flatworms, molluscs, ascidians and even some amphibians. Generally the animal host harbours a phototrophic partner, usually a cyanobacteria or a unicellular alga. An exception to this rule is found in some sea slugs, which only retain the chloroplasts of the algal food source and maintain them photosynthetically active in their own cytosol - a phenomenon called 'functional kleptoplasty'. Research has focused largely on the biodiversity of photosymbiotic species across a range of taxa. However, many questions with regard to the evolution of the ability to establish and maintain a photosymbiosis are still unanswered. To date, attempts to understand genome adaptations which could potentially lead to the evolution of photosymbioses have only been performed in cnidarians. This knowledge gap for other systems is mainly due to a lack of genetic information, both for non-symbiotic and symbiotic species. Considering non-photosymbiotic species is, however, important to understand the factors that make symbiotic species so unique. Herein we provide an overview of the diversity of photosymbioses across the animal kingdom and discuss potential scenarios for the evolution of this association in different lineages. We stress that the evolution of photosymbiosis is probably based on genome adaptations, which (i) lead to recognition of the symbiont to establish the symbiosis, and (ii) are needed to maintain the symbiosis. We hope to stimulate research involving sequencing the genomes of various key taxa to increase the genomic resources needed to understand the most fundamental question: how have animals evolved the ability to establish and maintain a photosymbiosis?

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Photosymbiosis in Marine Pelagic Environments

Cited by 16 publications

References 140 publications

Mixotrophy everywhere on land and in water: thegrand écarthypothesis

Mixotrophy everywhere on land and in water: thegrand écarthypothesis

Evolutionary significance of the microbial assemblages of large benthic Foraminifera

Polymorphic adaptations in metazoans to establish and maintain photosymbioses

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