Mixotrophy in microorganisms: Ecological and cytophysiological aspects

Matantseva, Olga; Skarlato, Sergei

doi:10.1134/s0022093013040014

Cited by 27 publications

(17 citation statements)

References 67 publications

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“…Far from a curiosity, many phytoplankton taxa have phagotrophic members, including numerous dinoflagellates, chrysophytes, cryptophytes, prasinophytes, and haptophytes (Sanders and Porter, 1988;Raven et al, 2009;Flynn et al, 2013). The great abundances of mixotrophs in most aquatic systems suggest this nutritional mode should be considered the rule rather than the exception (Matantseva and Skarlato, 2013).…”

Section: Introductionmentioning

confidence: 99%

Single-Cell View of Carbon and Nitrogen Acquisition in the Mixotrophic Alga Prymnesium parvum (Haptophyta) Inferred From Stable Isotope Tracers and NanoSIMS

et al. 2018

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Nutritional modes of unicellular eukaryotes range from pure photoautotrophy of some phytoplankton to pure heterotrophy of species typically called protozoa. Between these two extremes lies a functional continuum of nutrient and energy acquisition modes termed mixotrophy. Prymnesium parvum is an ecologically important mixotrophic haptophyte alga that can produce toxins and form ecosystem disruptive blooms that result in fish kills and changes in planktonic food web structure. We investigated carbon and nitrogen acquisition strategies of single cells of P. parvum using a combined experimental-imaging approach employing labeling of live cells with stable isotope tracers (13 C and 15 N) followed by measurement of cellular isotopic ratios using nanometer-scale secondary ion mass spectrometry (NanoSIMS). With this method, we were able to quantify the relative contributions of photosynthesis and heterotrophy to the nutrition of the alga. Our results suggest that P. parvum relies on predation primarily for nitrogen, while most carbon for cellular building blocks is obtained from inorganic sources. Our analysis further revealed that nitrogen assimilation can vary up to an order of magnitude among individual cells, a finding that would be difficult to determine using other methods. These results help to improve our understanding of mixotrophy across the enormous diversity of eukaryotes, one cell and one species at a time.

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Section: Introductionmentioning

confidence: 99%

Single-Cell View of Carbon and Nitrogen Acquisition in the Mixotrophic Alga Prymnesium parvum (Haptophyta) Inferred From Stable Isotope Tracers and NanoSIMS

et al. 2018

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“…As proposed in , most photosynthetic microorganisms seem to have the capacity for both inorganic (by photosynthesis) and organic (by respiration) carbon assimilation (Figs ), possibly to overcome inorganic macronutrient deficiencies. The regulation and mechanism of this particular metabolic capacity in cyanobacteria, which implies the contemporaneous activity of photosynthetic and respiratory reactions in both the same membrane and cytosolic compartment sharing the same electron carriers and amphibolic sequences, is insufficiently understood (for review see ).…”

Section: Discussionmentioning

confidence: 89%

“…The mixotrophic growth behaviour is widely spread among prokaryotes and protists . The physiological role of mixotrophy among photosynthetic microorganisms has been discussed by two different hypotheses: (a) assimilation of carbon when photosynthesis is severely restricted (e.g.…”

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confidence: 99%

“…The physiological role of mixotrophy among photosynthetic microorganisms has been discussed by two different hypotheses: (a) assimilation of carbon when photosynthesis is severely restricted (e.g. insufficient illumination), or (b) uptake of nitrogen or phosphorus under inorganic macronutrient‐deficient stress conditions . In the study, we evaluate the capacity of Thermosynechococcus elongatus BP‐1, a crucial thermophilic photosynthetic model organism, to assimilate organic carbon sources.…”

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Unexpected capacity for organic carbon assimilation by Thermosynechococcus elongatus, a crucial photosynthetic model organism

Zilliges

Dau

2016

FEBS Letters

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Genetic modification of key residues of photosystems is essential to identify functionally crucial processes by spectroscopic and crystallographic investigation; the required protein stability favours use of thermophilic species. The currently unique thermophilic photosynthetic model organism is the cyanobacterial genus Thermosynechococcus. We report the ability of Thermosynechococcus elongatus to assimilate organic carbon, specifically D-fructose. Growth in the presence of a photosynthesis inhibitor opens the door towards crucial amino acid substitutions in photosystems by the rescue of otherwise lethal mutations. Yet depression of batch-culture growth after 7 days implies that additional developments are needed.Keywords: carbon metabolism; cyanobacteria; mixotrophy and photoheterotrophy; photosystem II Two of the crucial protein complexes for life on earth are the photosystems (PS) of oxygenic photosynthesis, PSI and PSII (for review see [1]). Specifically the light-driven water splitting (water oxidation) by PSII is a hot spot of topical research, inter alia because PSII serves as a 'role model' for water oxidation in synthetic system for sustainable production of nonfossil fuels [2,3]. Thermophilic cyanobacteria play a key role in the endeavour to obtain a thorough mechanistic understanding of photosynthetic water oxidation. Their superior stability of the protein complexes has facilitated crystallisation and structure elucidation [4], first of PSI [5] and then of intact PSII [6][7][8]. Notably, crystallisation of intact PSII containing the active site of water oxidation, a proteinbound manganese-calcium-oxo cluster, has been achieved only for two closely related thermophilic cyanobacteria, specifically Thermosynechococcus elongatus and Thermosynechococcus vulcanus. Moreover, the superior thermostability of purified PSII from thermophilic cyanobacteria is highly favourable for spectroscopic investigations. However, there has been a serious drawback regarding the use of thermophilic cyanobacteria in photosynthesis research: These organisms are mostly believed to be incapable of growing in the absence of a functional PSII, rendering genetic modification of key amino acid residues impossible. The unexpected ability of T. elongatus to use external carbon sources for growing photoheterotrophically, without light-driven water oxidation by PSII, is the subject of our study.For many decades, most cyanobacteria including all thermophilic species such as T. elongatus have been considered as obligate photolithoautotrophic prokaryotes using light, H 2 O and solely CO 2 as energy, electron and carbon source respectively [9]. Just for a few mesophilic species, for example, Synechocystis sp. PCC 6803, the capacity for metabolisation of organic carbon sources, namely D-glucose, has been well known for a long time [10]. This ability of Synechocystis Abbreviations DCMU, 3-(3,4-dichlorophenyl)-1,1-dimethylurea; LAHG, light-activated heterotrophic growth; NDH-1 complex, bacterial-type I NAD(P)H-quinone oxidoreductase; OD 750 , ...

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“…Nitrifying organisms capable of mixotrophy may pose an advantage in a musselinfluenced habitat, owing to the adaptation of switching metabolic functions when conditions change from oxic to anoxic [237,238]. It was previously thought that nitrite (NO2 -) oxidizing bacteria (NOB) were restricted to oxic environments where ammonia (NH3) oxidizing bacteria (AOB) produce NO2 -, but recent genomic analyses have expanded the known metabolic functions of conventional NOB Nitrospira.…”

Section: Introductionmentioning

confidence: 99%

Assessing the impacts of native freshwater mussels on nitrogen cycling microbial communities using metagenomics

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Mixotrophy in microorganisms: Ecological and cytophysiological aspects

Cited by 27 publications

References 67 publications

Single-Cell View of Carbon and Nitrogen Acquisition in the Mixotrophic Alga Prymnesium parvum (Haptophyta) Inferred From Stable Isotope Tracers and NanoSIMS

Single-Cell View of Carbon and Nitrogen Acquisition in the Mixotrophic Alga Prymnesium parvum (Haptophyta) Inferred From Stable Isotope Tracers and NanoSIMS

Unexpected capacity for organic carbon assimilation by Thermosynechococcus elongatus, a crucial photosynthetic model organism

Assessing the impacts of native freshwater mussels on nitrogen cycling microbial communities using metagenomics

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