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Marc-andré Selosse - One of the best experts on this subject based on the ideXlab platform.
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Mixotrophy in Land Plants: Why To Stay Green?
Trends in plant science, 2018Co-Authors: Jakub Tĕšitel, Tamara Těšitelová, Julita Minasiewicz, Marc-andré SelosseAbstract:Mixotrophic plants combine photosynthesis and heterotrophic nutrition. Recent research suggests mechanisms explaining why Mixotrophy is so common in terrestrial ecosystems. First, Mixotrophy overcomes nutrient limitation and/or seedling establishment constraints. Second, although genetic drift may push mixotrophs to full heterotrophy, the role of photosynthesis in reproduction stabilizes Mixotrophy.
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The C-13 content of the orchid Epipactis palustris (L.) Crantz responds to light as in autotrophic plants
Botany Letters, 2018Co-Authors: Félix Lallemand, Pierre-emmanuel Courty, Alicja Robionek, Marc-andré SelosseAbstract:Most temperate green orchids form mycorrhizae with rhizoctonias fungi and are considered autotrophic. Some orchids, however, associate with fungi that also form ectomycorrhizae with surrounding trees and derive part of their carbon from these fungi. This evolutionarily derived condition, called Mixotrophy, is characterized by natural C-13 enrichment and high N content. Some orchid genera display both syndromes depending on species. Here, we further document the isotopic features of a rhizoctonias-associated species, Epipactis palustris, in a genus otherwise encompassing many mixotrophic orchids. First, E. palustris in two wetland sites from Northern Europe displayed similar to slightly-depleted C-13 abundance and identical N content as compared with surrounding autotrophic plants, confirming published results on this species. Second, some individuals growing in darker conditions (63% reduced irradiation) revealed a decrease of C-13 abundance as expected (and observed at the same place) for autotrophic plants. The latter result expands previous observations on other rhizoctonias-associated orchid species. We discuss our results in relationship with the current views of the two nutritional syndromes of green orchids (especially, with the doubts on autotrophy of rhizoctonias-associated species) and in the framework of the phylogeny of Epipactis that evolved secondarily Mixotrophy. The latter observation entails that the tribe Neottieae repeatedly evolved Mixotrophy.
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Mixotrophy in Pyroleae (Ericaceae) from Estonian boreal forests does not vary with light or tissue age
Annals of Botany, 2017Co-Authors: Félix Lallemand, Mait Lang, Aarne Luud, Pierre-emmanuel Courty, Cécile Palancade, Marc-andré SelosseAbstract:In temperate forests, some green plants, namely pyroloids (Pyroleae, Ericaceae) and some orchids, independently evolved a mode of nutrition mixing photosynthates and carbon gained from their mycorrhizal fungi (Mixotrophy). Fungal carbon is more enriched in 13C than photosynthates, allowing estimation of the proportion of carbon acquired heterotrophically from fungi in plant biomass. Based on 13C enrichment, mixotrophic orchids have previously been shown to increase shoot autotrophy level over the growth season and with environmental light availability. But little is known about the plasticity of use of photosynthetic versus fungal carbon in pyroloids. Methods : Plasticity of Mixotrophy with leaf age or light level (estimated from canopy openness) was investigated in pyroloids from three Estonian boreal forests. Bulk leaf 13C enrichment of five pyroloid species was compared with that of control autotrophic plants along temporal series (over one growth season) and environmental light gradients (n=405 samples). Key Results : Mixotrophic 13C enrichment was detected at studied sites for Pyrola chlorantha and Orthilia secunda (except at one site for the latter), but not for Chimaphila umbellata, Pyrola rotundifolia and Moneses uniflora. Enrichment with 13C did not vary over the growth season or between leaves from current and previous years. Finally, although one co-occurring mixotrophic orchid showed 13C depletion with increasing light availability, as expected for mixotrophs, all pyroloids responded identically to autotrophic control plants along light gradients. Conclusions : A phylogenetic trend previously observed is further supported: Mixotrophy is rarely supported by 13C enrichment in the Chimaphila + Moneses clade, whereas it is frequent in the Pyrola + Orthilia clade. Moreover, pyroloid Mixotrophy does not respond plastically to ageing or to light level. This contrasts with the usual view of a convergent evolution with orchids, and casts doubt on the way pyroloids use the carbon gained from their mycorrhizal fungi, especially to replace photosynthetic carbon
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Mixotrophy everywhere on land and in water: the grand écart hypothesis.
Ecology letters, 2016Co-Authors: Marc-andré Selosse, Marie Charpin, Fabrice NotAbstract: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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Mixotrophy in mycorrhizal plants : extracting C from mycorrhizal networks
2016Co-Authors: Marc-andré Selosse, Melissa Bocayuva, Maria Catarina Megumi Kasuya, Pierre-emmanuel CourtyAbstract:This chapter reviews the discovery of Mixotrophy in mycorrhizal plants, the available data on mixotrophic physiology, and the evolutionary link between Mixotrophy and full mycoheterotrophy. In usual mycorrhizal associations, the fungus exploits plant photosynthetic carbon (C) and provides mineral resources as a reward, such as nitrogen (N), phosphorous or water collected in the soil by its mycelium. A variant of mycoheterotrophy occurs in plants that initiate their development as mycoheterotrophic seedlings before turning green at adulthood. This initial mycoheterotrophy is known in several basal plant lineages disseminated by spores, but also in plants that form minute seeds with extremely limited reserves and require fungal C to germinate as mycoheterotrophs, such as orchids. Initial mycoheterotrophy may still fit into a mutualistic framework, since the fungus is rewarded in C when plants are adult. Mixo- and mycoheterotrophic plants offer a fascinating, newly and fully open research area, demonstrating the power of mycorrhizal networks in shaping mycorrhizal networks.
Edna Granéli - One of the best experts on this subject based on the ideXlab platform.
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Influence of Light on Prymnesium Parvum Growth, Toxicity and Mixotrophy
Linnaeus Eco-Tech, 2017Co-Authors: Emanuela Fiori, Nayani K. Vidyarathna, Johannes A. Hagström, Rossella Pistocchi, Edna GranéliAbstract:The haptophyte Prymnesium parvum has a worldwide distribution, with dramatic increase in blooms in the last years. P. parvum blooms are often associated with massive fish kills and great ecological impacts and economic losses as a consequence. P. parvum is a mixotrophic organism, utilizing organic dissolved substances and particles to support its photosynthetic growth. The ability of P. parvum to produce toxic compounds, and being a mixotroph, makes it capable to outcompete other algal species for essential substances. These mechanisms are mostly enhanced when environmental conditions are not optimal for P. parvum growth. Here we report results on the growth, toxicity and Mixotrophy, from experiments where P. parvum cells were grown as monocultures or together with Rhodomonas salina and exposed to different light conditions (dark, 100, 700, 2000 μmol photons m-2 s-1). The results showed that P. parvum growth is affected at light intensity of 700 μmol photons m-2 s-1 and the cells were photo-lysed when exposed to irradiances above this value. An inverse relationship between cellular toxicity and light intensity was observed, i.e. lower light irradiation induced higher cell toxicity. Phagotrophy was observed in all the conditions. P. parvum reached significantly higher cell densities when growing together with R. salina than in monocultures, while cellular toxicity was significantly reduced in the mixed cultures. Furthermore the presence of prey attenuated the negative effect of the higher irradiations on P. parvum growth.
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Role of Mixotrophy and light for growth and survival of the toxic haptophyte Prymnesium parvum
Harmful Algae, 2011Co-Authors: Andreas Brutemark, Edna GranéliAbstract:Mixotrophy in Prymnesium parvum was investigated using carbon (δ13C) and nitrogen (δ15N) stable isotopes. The experiment was performed in light and dark. In the dark treatment we expected that the ...
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Kill your enemies and eat them with the help of your toxins: an algal strategy
African Journal of Marine Science, 2006Co-Authors: Edna GranéliAbstract:Prymnesium spp. have been shown to kill both their grazers and other algal species, by producing allelopathic compounds. Killing nutrient-competing phytoplankton species enables Prymnesium to freely utilise limiting resources. Mixotrophy, i.e. the ability to ingest bacteria, other algae, and potential grazers, also contributes to the bloom-forming ability of Prymnesium spp. Allelopathy, Mixotrophy and grazer deterrence increase when cells of Prymnesium spp. are grown under N- or P-deficiency, as does toxicity. However, the opposite holds if cells are grown with excess N and P in proportions balanced to the needs of the alga. Prymnesium filtrates from nutrient-deficient cultures also exhibit strong allelopathy against other algal species and grazer deterrence. It seems that toxin production in Prymnesium spp. functions not only as a defence mechanism, but also serves to kill competitors, thereby increasing the ability to compete under conditions of nutrient depletion. A consequence of increasing the input ...
Aditee Mitra - One of the best experts on this subject based on the ideXlab platform.
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Mixotrophy in Harmful Algal Blooms: By Whom, on Whom, When, Why, and What Next
Ecological Studies, 2018Co-Authors: Kevin J. Flynn, Aditee Mitra, Patricia M. Glibert, Jo Ann M. BurkholderAbstract:The traditional view of the planktonic food web is simplistic: nutrients are consumed by phytoplankton that, in turn, support zooplankton, which ultimately support fish. This structure is the foundation of most models used to explore fisheries production, biogeochemical cycling, and climate change. In recent years, however, the importance of mixotrophs increasingly has been recognized. Mixotrophy, the combination of phototrophy and heterotrophy (the latter, including phago- and/or osmotrophy), enables planktonic protists traditionally labeled as “phytoplankton” or “microzooplankton” to function at multiple trophic levels. Mixotrophy enables primary producers to acquire nutrients directly from ingestion of prey such as bacteria and algal competitors and even from their own potential predators. Mixotrophy is not simply additive or substitutional; rather, it is synergistic. While most harmful algal species (except diatoms and cyanobacteria) are mixotrophic via phagotrophy, little is known about how these organisms modulate their phototrophic and phagotrophic activities or how the flow of energy and material through mixotrophic predator-prey interactions is altered under varying nutrient, temperature, light, pH, or pCO2 conditions. All of these factors are also rapidly changing in coastal and oceanic environments with accelerating eutrophication and climate change that, in turn, alters the potential for harmful algal blooms. Accurate parameterization, including consideration of Mixotrophy in water quality or fisheries models that are used as aids to regional and/or international policy development, should be a high priority.
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simulating effects of variable stoichiometry and temperature on Mixotrophy in the harmful dinoflagellate karlodinium veneficum
Frontiers in Marine Science, 2018Co-Authors: Chihhsien Lin, Aditee Mitra, Kevin J. Flynn, Patricia M. GlibertAbstract:Results from a dynamic mathematical model are presented simulating the growth of the harmful algal bloom (HAB) mixotrophic dinoflagellate Karlodinium veneficum and its algal prey, Rhodomonas salina. The model describes carbon-nitrogen-phosphorus-based interactions within the mixotroph, interlinking autotrophic and phagotrophic nutrition. The model was tuned to experimental data from these species grown under autotrophic conditions and in mixed batch cultures in which nitrogen:phosphorus stoichiometry (input molar N:P of 4, 16, and 32) of both predator and prey varied. A good fit was attained to all experimentally derived carbon biomass data. The potential effects of temperature and nutrient changes on promoting growth of prey and thus K. veneficum bloom formation were explored using this simulation platform. The simulated biomass of K. veneficum was highest when they were functioning as mixotrophs and when they consumed prey under elevated N:P conditions. The scenarios under low N:P responded differently, with simulations showing larger deviation between mixotrophic and autotrophic growth, depending on temperature. When inorganic nutrients were in balanced proportions, lower biomass of the mixotroph was attained at all temperatures in the simulations, suggesting that natural systems might be more resilient against Karlodinium HAB development in warming conditions if nutrients were available in balanced proportions. These simulations underscore the need for models of HAB dynamics to include consideration of prey; modeling HAB as autotrophs is insufficient. The simulations also imply that warmer, wetter springs that may bring more N with lower N:P, such as predicted under climate change scenarios for Chesapeake Bay, may be more conducive to development of these HABs. Prey availability may also increase with temperature due to differential growth temperature responses of K. veneficum and its prey.
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Oceanic protists with different forms of acquired phototrophy display contrasting biogeographies and abundance
Proceedings. Biological sciences, 2017Co-Authors: Suzanne Leles, Aditee Mitra, Robert W. Sanders, David A Caron, Kevin J. Flynn, Per Juel Hansen, Diane K. Stoecker, Albert Calbet, George B. Mcmanus, Fabrice NotAbstract:This first comprehensive analysis of the global biogeography of marine protistan plankton with acquired phototrophy shows these mixotrophic organisms to be ubiquitous and abundant; however, their biogeography differs markedly between different functional groups. These mixotrophs, lacking a constitutive capacity for photosynthesis (i.e. non-constitutive mixotrophs, NCMs), acquire their phototrophic potential through either integration of prey-plastids or through endosymbiotic associations with photosynthetic microbes. Analysis of field data reveals that 40–60% of plankton traditionally labelled as (non-phototrophic) microzooplankton are actually NCMs, employing acquired phototrophy in addition to phagotrophy. Specialist NCMs acquire chloroplasts or endosymbionts from specific prey, while generalist NCMs obtain chloroplasts from a variety of prey. These contrasting functional types of NCMs exhibit distinct seasonal and spatial global distribution patterns. Mixotrophs reliant on ‘stolen’ chloroplasts, controlled by prey diversity and abundance, dominate in high-biomass areas. Mixotrophs harbouring intact symbionts are present in all waters and dominate particularly in oligotrophic open ocean systems. The contrasting temporal and spatial patterns of distribution of different mixotroph functional types across the oceanic provinces, as revealed in this study, challenges traditional interpretations of marine food web structures. Mixotrophs with acquired phototrophy (NCMs) warrant greater recognition in marine research.
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Modeling plankton Mixotrophy: A mechanistic model consistent with the shuter-type biochemical approach
Frontiers in Ecology and Evolution, 2017Co-Authors: Caroline Ghyoot, Aditee Mitra, Kevin J. Flynn, Christiane Lancelot, Nathalie GypensAbstract:Mixotrophy, i.e., the ability to combine phototrophy and phagotrophy in one organism, is now recognized to be widespread among photic-zone protists and to potentially modify the structure and functioning of planktonic ecosystems. However, few biogeochemical/ecological models explicitly include this mode of nutrition, owing to the large diversity of observed mixotrophic types, the few data allowing the parameterization of physiological processes, and the need to make the addition of Mixotrophy into existing ecosystem models as simple as possible. We here propose and discuss a flexible model that depicts the main observed behaviors of Mixotrophy in microplankton. A first model version describes constitutive Mixotrophy (the organism photosynthesizes by use of its own chloroplasts). This model version offers two possible configurations, allowing the description of constitutive mixotrophs (CMs) that favor either phototrophy or heterotrophy. A second version describes non-constitutive Mixotrophy (the organism performs phototrophy by use of chloroplasts acquired from its prey). The model variants were described so as to be consistent with a plankton conceptualization in which the biomass is divided into separate components on the basis of their biochemical function (Shuter-approach; Shuter, 1979). The two model variants of Mixotrophy can easily be implemented in ecological models that adopt the Shuter-approach, such as the MIRO model (Lancelot et al., 2005), and address the challenges associated with modelling Mixotrophy.
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Mixotrophy in the marine plankton
Annual Review of Marine Science, 2017Co-Authors: Diane K. Stoecker, Per Juel Hansen, David A Caron, Aditee MitraAbstract:Mixotrophs are important components of the bacterioplankton, phytoplankton, microzooplankton, and (sometimes) zooplankton in coastal and oceanic waters. Bacterivory among the phytoplankton may be important for alleviating inorganic nutrient stress and may increase primary production in oligotrophic waters. Mixotrophic phytoflagellates and dinoflagellates are often dominant components of the plankton during seasonal stratification. Many of the microzooplankton grazers, including ciliates and Rhizaria, are mixotrophic owing to their retention of functional algal organelles or maintenance of algal endosymbionts. Phototrophy among the microzooplankton may increase gross growth efficiency and carbon transfer through the microzooplankton to higher trophic levels. Characteristic assemblages of mixotrophs are associated with warm, temperate, and cold seas and with stratification, fronts, and upwelling zones. Modeling has indicated that Mixotrophy has a profound impact on marine planktonic ecosystems and may enhan...
Diane K. Stoecker - One of the best experts on this subject based on the ideXlab platform.
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Oceanic protists with different forms of acquired phototrophy display contrasting biogeographies and abundance
Proceedings. Biological sciences, 2017Co-Authors: Suzanne Leles, Aditee Mitra, Robert W. Sanders, David A Caron, Kevin J. Flynn, Per Juel Hansen, Diane K. Stoecker, Albert Calbet, George B. Mcmanus, Fabrice NotAbstract:This first comprehensive analysis of the global biogeography of marine protistan plankton with acquired phototrophy shows these mixotrophic organisms to be ubiquitous and abundant; however, their biogeography differs markedly between different functional groups. These mixotrophs, lacking a constitutive capacity for photosynthesis (i.e. non-constitutive mixotrophs, NCMs), acquire their phototrophic potential through either integration of prey-plastids or through endosymbiotic associations with photosynthetic microbes. Analysis of field data reveals that 40–60% of plankton traditionally labelled as (non-phototrophic) microzooplankton are actually NCMs, employing acquired phototrophy in addition to phagotrophy. Specialist NCMs acquire chloroplasts or endosymbionts from specific prey, while generalist NCMs obtain chloroplasts from a variety of prey. These contrasting functional types of NCMs exhibit distinct seasonal and spatial global distribution patterns. Mixotrophs reliant on ‘stolen’ chloroplasts, controlled by prey diversity and abundance, dominate in high-biomass areas. Mixotrophs harbouring intact symbionts are present in all waters and dominate particularly in oligotrophic open ocean systems. The contrasting temporal and spatial patterns of distribution of different mixotroph functional types across the oceanic provinces, as revealed in this study, challenges traditional interpretations of marine food web structures. Mixotrophs with acquired phototrophy (NCMs) warrant greater recognition in marine research.
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Mixotrophy in the marine plankton
Annual Review of Marine Science, 2017Co-Authors: Diane K. Stoecker, Per Juel Hansen, David A Caron, Aditee MitraAbstract:Mixotrophs are important components of the bacterioplankton, phytoplankton, microzooplankton, and (sometimes) zooplankton in coastal and oceanic waters. Bacterivory among the phytoplankton may be important for alleviating inorganic nutrient stress and may increase primary production in oligotrophic waters. Mixotrophic phytoflagellates and dinoflagellates are often dominant components of the plankton during seasonal stratification. Many of the microzooplankton grazers, including ciliates and Rhizaria, are mixotrophic owing to their retention of functional algal organelles or maintenance of algal endosymbionts. Phototrophy among the microzooplankton may increase gross growth efficiency and carbon transfer through the microzooplankton to higher trophic levels. Characteristic assemblages of mixotrophs are associated with warm, temperate, and cold seas and with stratification, fronts, and upwelling zones. Modeling has indicated that Mixotrophy has a profound impact on marine planktonic ecosystems and may enhan...
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Mixotrophy in the Marine Plankton
Annual review of marine science, 2016Co-Authors: Diane K. Stoecker, Per Juel Hansen, David A Caron, Aditee MitraAbstract:Mixotrophs are important components of the bacterioplankton, phytoplankton, microzooplankton, and (sometimes) zooplankton in coastal and oceanic waters. Bacterivory among the phytoplankton may be important for alleviating inorganic nutrient stress and may increase primary production in oligotrophic waters. Mixotrophic phytoflagellates and dinoflagellates are often dominant components of the plankton during seasonal stratification. Many of the microzooplankton grazers, including ciliates and Rhizaria, are mixotrophic owing to their retention of functional algal organelles or maintenance of algal endosymbionts. Phototrophy among the microzooplankton may increase gross growth efficiency and carbon transfer through the microzooplankton to higher trophic levels. Characteristic assemblages of mixotrophs are associated with warm, temperate, and cold seas and with stratification, fronts, and upwelling zones. Modeling has indicated that Mixotrophy has a profound impact on marine planktonic ecosystems and may enhance primary production, biomass transfer to higher trophic levels, and the functioning of the biological carbon pump.
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Defining Planktonic Protist Functional Groups on Mechanisms for Energy and Nutrient Acquisition: Incorporation of Diverse Mixotrophic Strategies
Protist, 2016Co-Authors: Aditee Mitra, David A Caron, John A. Raven, Kevin J. Flynn, Urban Tillmann, Gustaaf M. Hallegraeff, Per Juel Hansen, Diane K. Stoecker, Robert W. SandersAbstract:Arranging organisms into functional groups aids ecological research by grouping organisms (irrespective of phylogenetic origin) that interact with environmental factors in similar ways. Planktonic protists traditionally have been split between photoautotrophic "phytoplankton" and phagotrophic "microzooplankton". However, there is a growing recognition of the importance of Mixotrophy in euphotic aquatic systems, where many protists often combine photoautotrophic and phagotrophic modes of nutrition. Such organisms do not align with the traditional dichotomy of phytoplankton and microzooplankton. To reflect this understanding, we propose a new functional grouping of planktonic protists in an eco-physiological context: (i) phagoheterotrophs lacking phototrophic capacity, (ii) photoautotrophs lacking phagotrophic capacity, (iii) constitutive mixotrophs (CMs) as phagotrophs with an inherent capacity for phototrophy, and (iv) non-constitutive mixotrophs (NCMs) that acquire their phototrophic capacity by ingesting specific (SNCM) or general non-specific (GNCM) prey. For the first time, we incorporate these functional groups within a foodweb structure and show, using model outputs, that there is scope for significant changes in trophic dynamics depending on the protist functional type description. Accordingly, to better reflect the role of Mixotrophy, we recommend that as important tools for explanatory and predictive research, aquatic food-web and biogeochemical models need to redefine the protist groups within their frameworks.
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The impact of Mixotrophy on planktonic marine ecosystems
Ecological Modelling, 1999Co-Authors: H.l. Stickney, Raleigh R. Hood, Diane K. StoeckerAbstract:Abstract Mixotrophic protists, which utilize a nutritional strategy that combines phototrophy and phagotrophy, are commonly found in fresh, estuarine, and oceanic waters at all latitudes. A number of different physiological types of mixotrophs are possible, including forms which are able to use both phototrophy and phagotrophy equally well, primarily phototrophic phagocytic ‘algae’, and predominantly heterotrophic photosynthetic ‘protozoa’. Mixotrophs are expected to have important effects on the trophic dynamics of ecosystems, but the exact nature of these effects is not known and likely varies with physiological type. In order to study the impact that mixotrophs may have on the microbial food web, we developed mathematical formulations that simulate each of the three aforementioned physiological types of mixotrophs. These were introduced into idealized, steady-state open ocean and coastal/estuarine environments. Our results indicate that mixotrophs compete for resources with both phytoplankton and zooplankton and that their relative abundance is a function of the feeding strategy (physiological type and whether or not they feed on zooplankton) and the maximum growth and/or grazing rates of the organisms. In our models coexistence of mixotrophs with phytoplankton and zooplankton generally occurs within reasonable parameter ranges, which suggests that Mixotrophy represents a unique resource niche under summertime, quasi-steady state conditions. We also find that the introduction of mixotrophs tends to decrease the primary production based on uptake of nitrogen from the dissolved inorganic nitrogen pool, but that this decrease may be compensated for by mixotrophic primary production based upon organic nitrogen sources.
Robert W. Sanders - One of the best experts on this subject based on the ideXlab platform.
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Mixotrophic activity and diversity of Antarctic marine protists in austral summer
Frontiers in Marine Science, 2018Co-Authors: Rebecca J. Gast, Scott A. Fay, Robert W. SandersAbstract:Identifying putative mixotrophic protist species in the environment is important for understanding their behavior, with the recovery of these species in culture essential for determining the triggers of feeding, grazing rates and overall impact on bacterial standing stocks. In this project, mixotroph abundances determined using tracer ingestion in water and sea ice samples collected in the Ross Sea, Antarctica during the summer of 2011 were compared with data from the spring (Ross Sea) and fall (Arctic) to examine the impacts of bacterivory/Mixotrophy. Mixotrophic nanoplankton were usually less abundant than heterotrophs, but consumed more of the bacterial standing stock per day due to relatively higher ingestion rates (1-7 bacteria mixotroph-1 h-1 vs. 0.1-4 bacteria heterotroph-1 h-1). Yet, even with these high rates observed in the Antarctic summer, mixotrophs appeared to have a smaller contribution to bacterivory than in the Antarctic spring. Additionaly, putative mixotroph taxa were identified through incubation experiments accomplished with bromodeoxyuridine labeled bacteria as food, immunoprecipitation (IP) of labeled DNA, and amplification and high throughput sequencing of the eukaryotic ribosomal V9 region. Putative mixotroph OTUs were identified in the IP samples by taxonomic similarity to known phototroph taxa. OTUs that had increased abundance in IP samples compared to the non-IP samples from both surface and chlorophyll maximum (CM) depths were considered to represent active Mixotrophy and include ones taxonomically similar to Dictyocha, Gymnodinium, Pentapharsodinium and Symbiodinium. These OTUs represent target taxa for isolation and laboratory experiments on triggers for Mixotrophy, to be combined with qPCR to estimate their abundance, seasonal distribution and potential impact.
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Oceanic protists with different forms of acquired phototrophy display contrasting biogeographies and abundance
Proceedings. Biological sciences, 2017Co-Authors: Suzanne Leles, Aditee Mitra, Robert W. Sanders, David A Caron, Kevin J. Flynn, Per Juel Hansen, Diane K. Stoecker, Albert Calbet, George B. Mcmanus, Fabrice NotAbstract:This first comprehensive analysis of the global biogeography of marine protistan plankton with acquired phototrophy shows these mixotrophic organisms to be ubiquitous and abundant; however, their biogeography differs markedly between different functional groups. These mixotrophs, lacking a constitutive capacity for photosynthesis (i.e. non-constitutive mixotrophs, NCMs), acquire their phototrophic potential through either integration of prey-plastids or through endosymbiotic associations with photosynthetic microbes. Analysis of field data reveals that 40–60% of plankton traditionally labelled as (non-phototrophic) microzooplankton are actually NCMs, employing acquired phototrophy in addition to phagotrophy. Specialist NCMs acquire chloroplasts or endosymbionts from specific prey, while generalist NCMs obtain chloroplasts from a variety of prey. These contrasting functional types of NCMs exhibit distinct seasonal and spatial global distribution patterns. Mixotrophs reliant on ‘stolen’ chloroplasts, controlled by prey diversity and abundance, dominate in high-biomass areas. Mixotrophs harbouring intact symbionts are present in all waters and dominate particularly in oligotrophic open ocean systems. The contrasting temporal and spatial patterns of distribution of different mixotroph functional types across the oceanic provinces, as revealed in this study, challenges traditional interpretations of marine food web structures. Mixotrophs with acquired phototrophy (NCMs) warrant greater recognition in marine research.
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Defining Planktonic Protist Functional Groups on Mechanisms for Energy and Nutrient Acquisition: Incorporation of Diverse Mixotrophic Strategies
Protist, 2016Co-Authors: Aditee Mitra, David A Caron, John A. Raven, Kevin J. Flynn, Urban Tillmann, Gustaaf M. Hallegraeff, Per Juel Hansen, Diane K. Stoecker, Robert W. SandersAbstract:Arranging organisms into functional groups aids ecological research by grouping organisms (irrespective of phylogenetic origin) that interact with environmental factors in similar ways. Planktonic protists traditionally have been split between photoautotrophic "phytoplankton" and phagotrophic "microzooplankton". However, there is a growing recognition of the importance of Mixotrophy in euphotic aquatic systems, where many protists often combine photoautotrophic and phagotrophic modes of nutrition. Such organisms do not align with the traditional dichotomy of phytoplankton and microzooplankton. To reflect this understanding, we propose a new functional grouping of planktonic protists in an eco-physiological context: (i) phagoheterotrophs lacking phototrophic capacity, (ii) photoautotrophs lacking phagotrophic capacity, (iii) constitutive mixotrophs (CMs) as phagotrophs with an inherent capacity for phototrophy, and (iv) non-constitutive mixotrophs (NCMs) that acquire their phototrophic capacity by ingesting specific (SNCM) or general non-specific (GNCM) prey. For the first time, we incorporate these functional groups within a foodweb structure and show, using model outputs, that there is scope for significant changes in trophic dynamics depending on the protist functional type description. Accordingly, to better reflect the role of Mixotrophy, we recommend that as important tools for explanatory and predictive research, aquatic food-web and biogeochemical models need to redefine the protist groups within their frameworks.
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Physiological Responses of Three Species of Antarctic Mixotrophic Phytoflagellates to Changes in Light and Dissolved Nutrients
Microbial Ecology, 2015Co-Authors: Zaid M Mckie-krisberg, Rebecca J. Gast, Robert W. SandersAbstract:Antarctic phototrophs are challenged by extreme temperatures, ice cover, nutrient limitation, and prolonged periods of darkness. Yet this environment may also provide niche opportunities for phytoplankton utilizing alternative nutritional modes. Mixotrophy, the combination of photosynthesis and particle ingestion, has been proposed as a mechanism for some phytoplankton to contend with the adverse conditions of the Antarctic. We conducted feeding experiments using fluorescent bacteria-sized tracers to compare the effects of light and nutrients on bacterivory rates in three Antarctic marine photosynthetic nanoflagellates representing two evolutionary lineages: Cryptophyceae ( Geminigera cryophila ) and Prasinophyceae ( Pyramimonas tychotreta and Mantoniella antarctica ). Only G. cryophila had previously been identified as mixotrophic. We also measured photoautotrophic abilities over a range of light intensities (P vs. I) and used dark survival experiments to assess cell population dynamics in the absence of light. Feeding behavior in these three nanoflagellates was affected by either light, nutrient levels, or a combination of both factors in a species-specific manner that was not conserved by evolutionary lineage. The different responses to environmental factors by these mixotrophs supported the idea of tradeoffs in the use of phagotrophy and phototrophy for growth.
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Phagotrophy by the picoeukaryotic green alga Micromonas: implications for Arctic Oceans
The ISME Journal, 2014Co-Authors: Zaid M Mckie-krisberg, Robert W. SandersAbstract:Photosynthetic picoeukaryotes (PPE) are recognized as major primary producers and contributors to phytoplankton biomass in oceanic and coastal environments. Molecular surveys indicate a large phylogenetic diversity in the picoeukaryotes, with members of the Prymnesiophyceae and Chrysophyseae tending to be more common in open ocean waters and Prasinophyceae dominating coastal and Arctic waters. In addition to their role as primary producers, PPE have been identified in several studies as mixotrophic and major predators of prokaryotes. Mixotrophy, the combination of photosynthesis and phagotrophy in a single organism, is well established for most photosynthetic lineages. However, green algae, including prasinophytes, were widely considered as a purely photosynthetic group. The prasinophyte Micromonas is perhaps the most common picoeukaryote in coastal and Arctic waters and is one of the relatively few cultured representatives of the picoeukaryotes available for physiological investigations. In this study, we demonstrate phagotrophy by a strain of Micromonas (CCMP2099) isolated from Arctic waters and show that environmental factors (light and nutrient concentration) affect ingestion rates in this mixotroph. In addition, we show size-selective feeding with a preference for smaller particles, and determine P vs I (photosynthesis vs irradiance) responses in different nutrient conditions. If other strains have mixotrophic abilities similar to Micromonas CCMP2099, the widespread distribution and frequently high abundances of Micromonas suggest that these green algae may have significant impact on prokaryote populations in several oceanic regimes.
