Yeast Rhodotorula Rubra Research Articles

ИЗУЧЕНИЕ АНТИМИКРОБНОЙ АКТИВНОСТИ ЭКСТРАКТОВ МОЖЖЕВЕЛЬНИКА И ИХ ВЛИЯНИЕ НА МИКРОБНУЮ КОНТАМИНАЦИЮ ХЛЕБОБУЛОЧНЫХ ИЗДЕЛИЙ

The purpose of the study is to determine the antimicrobial activity of extracts of juniper berries and needles and their effect on microbial contamination of bakery products by microscopic fungi. In the course of the work, experimental extracts from juniper berries and needles with various concentrations were obtained, the antimicrobial activity of experimental extracts was assessed on strains of yeast Candida tropicalis, Saccharomyces cerevisiae, Rhodotorula rubra and bacteria Bacillus subtilis and Escherichia coli, as well as test baking of bread and its implementation. storage for further assessment of the effect of the studied concentrations of extracts on microbial contamination and shelf life of products. The extractants used to obtain experimental extracts were water and an aqueous solution of 50 % alcohol. The antimicrobial activity of the experimental extracts was assessed using the disk-diffusion method; dry nutrient media GMF and Sabouraud were used for the growth of microorganisms. The results of assessing the antimicrobial activity of the experimental extracts showed that none of the obtained extracts affected the growth of yeast strains. Aqueous and hydroalcoholic extracts of juniper needles at a concentration of 25 % showed inhibition of the growth of Bacillus subtilis and Escherichia coli bacteria. After test baking on a prototype bread with an aqueous extract of juniper needles, 25 % growth of mold fungi was detected after 72 hours of storage. No fungal growth was detected on the sample with a hydroalcoholic extract of juniper needles after 96 hours of storage.

Macrocystis pyrifera Extract Residual as Nutrient Source for the Production of Sophorolipids Compounds by Marine Yeast Rhodotorula rubra.

Seaweed processing generates liquid fraction residual that could be used as a low-cost nutrient source for microbial production of metabolites. The Rhodotorula strain is able to produce antimicrobial compounds known as sophorolipids. Our aim was to evaluate sophorolipid production, with antibacterial activity, by marine Rhodotorula rubra using liquid fraction residual (LFR) from the brown seaweed Macrocystis pyrifera as the nutrient source. LFR having a composition of 32% w/w carbohydrate, 1% w/w lipids, 15% w/w protein and 52% w/w ash. The best culture condition for sophorolipid production was LFR 40% v/v, without yeast extract, artificial seawater 80% v/v at 15 °C by 3 growth days, with the antibacterial activity of 24.4 ± 3.1 % on Escherichia coli and 21.1 ± 3.8 % on Staphylococcus aureus. It was possible to identify mono-acetylated acidic and methyl ester acidic sophorolipid. These compounds possess potential as pathogen controllers for application in the food industry.

Microscopic fungi of lithobiont communities of Argentine Islands Region: Data from the 22nd Ukrainian Antarctic Expedition

The identification of the diversity of microscopic fungi of lithobiont communities of the Argentine Islands in specimens collected during the 22nd Ukrainian Antarctic Expedition was the purpose of this work. Samples of rock, soil, mosses and lichens of rock micro-habitats of “Crustose lichen sub-formation and fruticose lichen and moss cushion sub-formation” were used in the work. These samples were used for extracting and cultivation of filamentous fungi on dense nutrient media. Determination of physiological and biochemical characteristics and identification of yeast-like fungi were performed using a microbiological analyser ‘Vitek-2’ (‘Bio Merieux’, France). Cultivation of microorganisms was carried out at temperatures from +2 to +37 °C. In results cultures of microscopic fungi of Zygomycota (Mucor circinelloides), Ascomycota (species of the genera cf. Tlielebolus, Talaromyces), representatives of the Anamorphic fungi group (Geomyces pannorum, species of the genera Alternaria, Acremonium, Aspergillus, Penicillium, and Cladosporium) were isolated from Antarctic samples. Microscopic fungi Penicillium spp. were dominated after the frequency in the studied samples (54.5%). Rhodotorula rubra and Candida sp. among isolated yeast fungi, and dark pigmented fungi represented by Aureobasidium pulhdans and Exophiala spp. were identified. The biological properties of a number of isolated fungi (the potential ability to synthesise important biologically active substances: melanins, carotenoids, lipids) are characterised. Mycobiota of rock communities of Argentine Islands is rich on filamentous and yeast fungi similarly to other regions of Antarctica. A number of fungi investigated are potentially able to synthesise biologically active substances. The dark pigmented species of the genera Cladosporium, Exophiala, Aureobasidium pulhdans, capable of melanin synthesis; ‘red’ yeast Rhodotorula rubra (carotenoid producers and resistant to toxic metals); Mucor circinelloides and Geomyces pannorum, lipid producers, are among these fungi. Yeast-like fungi assimilated a wide range of carbohydrates, which will allow them to be further used for cultivation in laboratory and process conditions. The collection of technologically promising strains of microorganisms, part of the Culture Collection of Fungi at Taras Shevchenko National University of Kyiv (Ukraine), is updated with isolated species (strains) of filamentous fungi and yeast – potential producers of biologically active substances, obtained within this study.

Biodegradation of chlorpyrifos and 3,5,6-trichloro-2-pyridinol by the epiphytic yeasts Rhodotorula glutinis and Rhodotorula rubra.

The possible involvement of the epiphytic yeasts Rhodotorula glutinis and Rhodotorula rubra in the biodegradation of the insecticide chlorpyrifos and its metabolite 3,5,6-trichloro-2-pyridinol (TCP), in pure cultures and in plant surfaces (tomato fruits) was investigated. Higher biodegradation rates were observed as the concentration of chlorpyrifos and the inoculum of the microorganisms were increased, while the yeasts proved to be more active at 25 and 15 °C. The presence of glucose in the mineral nutrient medium, as an extra source of carbon, delayed the biodegradation by Rhodotorula glutinis, while Rhodotorula rubra proved to be more active. The detection and quantification of the parent compound and TCP was successfully achieved using a LC/MS/MS chromatographic system. The in vitro enzymatic assays applied suggested that esterases may be involved in the biodegradation of chlorpyrifos, a fact that was further enhanced after the addition of the synergists triphenyl phosphate, diethyl maleate and piperonyl butoxide in the biodegradation trials. The decrease of chlorpyrifos residues on tomato fruits confirmed the corresponding on pure cultures, resulting in the suggestion that the yeasts R. glutinis and R. rubra can possibly be used successfully for the removal or detoxification of chlorpyrifos residues on tomatoes.

Carotenoid production in sugarcane juice and synthetic media supplemented with nutrients by Rhodotorula rubra l02.

In order for the use of biological carotenoids to become feasible, it is necessary to have adequate low cost sources and improved methods of cultivation. The aim of this study was to evaluate the effect of supplementation with nitrogen, phosphorus, zinc, and magnesium, on the biomass and carotenoid volumetric production by yeast Rhodotorula rubra L02 using a complex medium (sugarcane juice) and synthetic media (sucrose and maltose) as substrates. The experimental design used for each substrate was randomized in blocks with 16 treatments and 3 repetitions. The treatments were compound for 15 different combinations of nutrients (N; Mg; Zn; P, N + Mg; N + Zn; N + P; Mg + Zn; Mg + P; Zn + P; N + P + Zn; N + P + Mg; N + Zn + Mg; P + Zn + Mg; N + Zn + Mg + P) alone and combined, and a control. The results were submitted to analysis of variance and Tukey test at 5% significance level. Among the treatments evaluated, the highest production of dry biomass, with both maltose and sucrose, was observed for Mg (1.60 g/L and 1.94 g/L, respectively). Additionally, another treatment that stood out in terms of biomass production was the control treatment with maltose (1.54 g/L). After the incubation time, killer activity was not observed since there was no formation of inhibition halo around the L02 yeast.

β-carotene production from soap stock by loofa-immobilized Rhodotorula rubra in an airlift photobioreactor

Abstract In this study, the soap stock as a sole carbon source was used for growing a carotenoid producing yeast (Rhodotorula rubra). The application of soap stock resulted in increase of carotenoids yield up to 5.36 folds when compared with the grown cultures on glucose. On the best Monod equation fitted on the specific growth rate (μ) data, the maximum specific growth rate (μm) and half-saturation concentration (KS) were respectively determined at 0.064 h−1 and 3.26 g L−1 for total fatty acids presented in soap stock. Further tests on the carotenogenesis process were carried out in a cell-immobilized airlift photobioreactor where the natural loofa sponge was used for immobilization of the cells. The performance of the bioreactor was statistically studied by the response surface methodology (RSM) where aeration rate of 0.11 vvm and light irradiation intensity of 2517 Lx provided an optimum condition for producing β-carotene with a specific production rate of 22.65 mg gcell−1 day−1.

Antimicrobial Activity of Xanthohumol and Its Selected Structural Analogues.

The objective of this study was to evaluate the antimicrobial activity of structural analogues of xanthohumol 1, a flavonoid compound found in hops (Humulus lupulus). The agar-diffusion method using filter paper disks was applied. Biological tests performed for selected strains of Gram-positive (Staphylococcus aureus) and Gram-negative (Escherichia coli) bacteria, fungi (Alternaria sp.), and yeasts (Rhodotorula rubra, Candida albicans) revealed that compounds with at least one hydroxyl group—all of them have it at the C-4 position—demonstrated good activity. Our research showed that the strain S. aureus was more sensitive to chalcones than to the isomers in which the heterocyclic ring C is closed (flavanones). The strain R. rubra was moderately sensitive to only one compound: 4-hydroxy-4’-methoxychalcone 8. Loss of the hydroxyl group in the B-ring of 4’-methoxychalcones or its replacement by a halogen atom (−Cl, −Br), nitro group (−NO2), ethoxy group (−OCH2CH3), or aliphatic substituent (−CH3, −CH2CH3) resulted in the loss of antimicrobial activity towards both R. rubra yeast and S. aureus bacteria. Xanthohumol 1, naringenin 5, and chalconaringenin 7 inhibited growth of S. aureus, whereas 4-hydroxy-4′-methoxychalcone 8 was active towards two strains: S. aureus and R. rubra.

The effectiveness of various biological control agents on blister blight disease (Exobasidium vexans Massee) on tea

In order to obtain an effective, efficient, and environmentally sound biological control method of blister blight disease (Exobasidium vexans Massee) on tea, a field trial has been conducted to know the effectiveness of various antagonistic microorganisms as biological control agents, on blister blight disease. The trial was carried out at Ciliwung Tea Plantation (1.400 m asl), Bogor, West Java, designed in randomized complete block (RCB), with 7 treatments and 3 replications. The treatments tested comprised 2 filamentous fungi (molds): Verticillium sp. and JD (unidentified); yeast: Rhodotorula rubra; 2 bacteria: B5 (unidentified) and Bacillus subtilis; copper-chemical fungicide as a standard treatment; and control. The biological control agents and fungicide were sprayed on tea bushes infected by blister blight disease, and the parameter observed was blister blight disease intensity, which was formulated in percentage of disease intensity index (DII). The results showed that in heavy-attack condition (disease intensity index higher than 50%), only yeast Rhodotorula rubra which was effective in suppressing blister blight disease intensity on tea, up to 22%. Meanwhile, the others treatments of antagonistic microorganisms could not suppress the disease intensity, even the copper-chemical fungicide as a standard treatment was no longer effective too.

Fungi isolated from Niedźwiedzia Cave in Kletno (Lower Silesia, Poland)

Niedźwiedzia Cave is the most beautiful cave in Poland, discovered in a block of Cambrian marbles. It is the most important part of the reserve established in 1977. The cave is located within the Klodzko Valley, in Śnieznik Mt. Massif, in Kleśnica Stream Valley and was discovered in 1966 while working in a quarry. The study aimed at first mycological evaluation of the air and the rocks in Niedźwiedzia Cave. Nine species of filamentous fungi and a yeast species were isolated from the air sampled in the cave, whereas from the rocks - nine species of filamentous fungi and two species of yeasts were collected. Rhizopus stolonifer was the species most frequently isolated from the air and from the rocks, while the least isolated from the air was Sclerotinia sclerotiorum. Among the species found in the rock, the least frequently collected were Fusarium oxysporum and the yeast Rhodotorula rubra.

Synthesis and antimicrobial activity of some bisoctahydroxanthene-1,8-dione derivatives

The bisoctahydroxanthen-1,8-dione derivatives were synthesized effectively via p-dodecylbenzene sulfonic acid the catalysed cyclocondensation of cyclic 1,3-dicarbonyl compounds with 1,3- or 1,4-benzene dicarboxaldehydes in water. The products were obtained with yield ranged from 75 to 95%. The structures of compounds were characterized by FT-IR, 1H-NMR and elemental analysis. The antimicrobial properties of compounds against pathogens were investigated by the disc-diffusion method. These compounds were evaluated for potential antimicrobial activity against Gram-positive (Staphylococcus aureus, Bacillus cereus, S. epidermidis and Nocardia canis), Gram-negative bacteria (Escherichia coli, Proteus vulgaris and Pseudomonas aeroginosa), yeasts (Candida albicans and Rhodotorula rubra) and mold (Aspergillus niger). The growth of S. aureus, B. cereus, S. epidermidis, E. coli, C. albicans, R. rubra and A. niger were inhibited by 3f and 3g compounds. All compounds were resistant against Gram-negative bacteria (Proteus vulgaris and Pseudomonas aerginosa) and results were upon comparison with reference discs.

Production of curcuminoids by Escherichia coli carrying an artificial biosynthesis pathway

Curcuminoids, which are produced specifically by plants of the order Zingiberales, have long been used as food additives because of their aromatic, stimulant and colouring properties and as traditional Asian medicines because of their anti-tumour, antioxidant and hepatoprotective activities. Curcuminoids are therefore attractive targets for metabolic engineering. An artificial curcuminoid biosynthetic pathway, including reactions of phenylalanine ammonia-lyase (PAL) from the yeast Rhodotorula rubra, 4-coumarate : CoA ligase (4CL) from Lithospermum erythrorhizon and curcuminoid synthase (CUS) from rice (Oryza sativa), a type III polyketide synthase, was constructed in Escherichia coli for the production of curcuminoids. Cultivation of the recombinant E. coli cells in the presence of tyrosine or phenylalanine, or both, led to production of bisdemethoxycurcumin, dicinnamoylmethane and cinnamoyl-p-coumaroylmethane. Another E. coli system carrying 4CL and CUS genes was also used for high-yield production of curcuminoids from exogenously supplemented phenylpropanoid acids: p-coumaric acid, cinnamic acid and ferulic acid. The yields of curucminoids were up to approximately 100 mg l(-1). Furthermore, this system gave approximately 60 mg curcumin l(-1) from 10 g rice bran pitch, an industrial waste discharged during rice edible oil production, as a source of ferulic acid.

Exopolysaccharides produced by mixed culture of yeast Rhodotorula rubra GED10 and yogurt bacteria (Streptococcus thermophilus 13a + Lactobacillus bulgaricus 2-11)

The studies of the production of exopolysaccharides by lactose-negative yeast and a yogurt starter co-cultivated in a natural substrate containing lactose may be considered of interest because they reveal the possibilities for high-efficiency synthesis of biopolymers by mixed cultivation. The mixed culture Rhodotorula rubra GED10 + (Streptococcus thermophilus 13a + Lactobacillus bulgaricus 2-11) was cultivated in cheese whey ultrafiltrate (WU) (44.0 g lactose l(-1)) at initial pH 6.0, 28 degrees C, under intensive aeration (air-flow rate 1.0 l l(-1) min(-1), agitation 220 rev min(-1)) in a MBR AG fermentor. The mixed culture manifested the highest activity for synthesis of exopolysaccharides (19.3 g l(-1)) and cell mass (21.0 g l(-1)) at the 84th hour. The yogurt starter synthesized neutral exopolysaccharides, while the mixed culture yeast + yogurt starter produced acidic exopolysaccharides containing uronic acid (6%). The neutral sugar composition was identified as mannose, glucose, galactose, xylose and arabinose. Mannose dominated in the polymer composition (83%) that was produced only by the yeast (97%). Lactose in the WU can be effectively utilized by a co-culture of lactose-negative yeast-yogurt starter for synthesis of exopolysaccharides. The present findings propose an alternative use of WU as a cost-effective carbohydrate substrate, and suggest that the lactose-negative yeast Rhodotorula rubra can have industrial application as producers of exopolysaccharides.

Use of whey ultrafiltrate as a substrate for production of carotenoids by the yeast Rhodotorula rubra.

Carotenogenesis of the lactose-negative yeast Rhodotorula rubra GED5 was studied by cocultivation with Kluyveromyces lactis MP11 in whey ultrafiltrate (WU) (35, 50, and 70 g of lactose/L). Maximum yields of cell mass (24.3 g/L) and carotenoids (10.2 mg/L of culture fluid or 0.421 micro g/g of dry cells) were obtained by growing the microbial association in WU (50 g of lactose/L) in a fermentor with an airflow rate of 0.8 L/(L.min), agitation of 220 rpm, and temperature of 30 degrees C. The identified carotenoid pigments-beta-carotene, torulene, and torularhodin-reached maximum concentrations (133, 26.9, and 222.3 microg/g of dry cells, respectively) on d 5 for torulene and d 6 for beta-carotene and torularhodin.

Carotenoid production by lactoso-negative yeasts co-cultivated with lactic acid bacteria in whey ultrafiltrate.

Two strains were selected--the lactoso-negative yeast Rhodotorula rubra GED2 and the homofermentative Lactobacillus casei subsp. casei Ha1 for co-cultivation in cheese whey ultrafiltrate (WU) and active synthesis of carotenoids. Under conditions of intensive aeration (1.0 l/l min, 220 rpm), a temperature of 30 degrees C, WU with 55.0 g lactose/l, initial pH = 5.5, the carotenoid content in the cells reached a maximum, when the growth of the cultures had come to an end, i.e. in the stationary phase of the yeast. The maxima for dry cell accumulation (27.0 g/l) and carotenoid formation (12.1 mg/l culture medium) did not coincide on the 5th and 6th day, respectively. A peculiarity of the carotenoid-synthesizing Rh. rubra GED2 strain, co-cultivated with L. casei Ha1, was the production of carotenoids with high beta-carotene content (46.6% of total carotenoids) and 10.7% and 36.9% for torulene and torularhodin, respectively.

Biodegradation of plasticizers by Rhodotorula rubra

The degradation of plasticizers by the yeast Rhodotorula rubra J-96-1 (American Type Culture Collection 9449) in the presence of glucose was studied. The plasticizers included the commonly used bis-2-ethylhexyl adipate (B(EH)A), dioctyl phthalate (DOP), and dioctyl terephthalate (DOTP), and the less commonly used dipropylene glycol dibenzoate (D(PG)DB) and diethylene glycol dibenzoate (D(EG)DB). The proposal had been made that the latter two plasticizers be used as alternatives to the first three, which have been associated with negative environmental impacts. The degradation of D(PG)DB or D(EG)DB led to a significant increase in solution toxicity, which was associated with the production of metabolites resulting from the incomplete breakdown of the plasticizers. The toxic metabolites in the D(PG)DB system were identified as isomers of dipropylene glycol monobenzoate. A pathway for the formation of this metabolite was proposed. The metabolite observed when D(EG)DB was being degraded was tentatively identified as diethylene glycol monobenzoate by analogy to the D(PG)DB system. In contrast, no metabolites were observable and toxicity did not increase in the media during the degradation of B(EH)A, DOP, or DOTP by R. rubra. Collectively, these results do not support the use of D(PG)DB and D(EG)DB as environmentally safe alternatives to B(EH)A, DOP, or DOTP.

Heterologous production of flavanones in Escherichia coli: potential for combinatorial biosynthesis of flavonoids in bacteria.

Chalcones, the central precursor of flavonoids, are synthesized exclusively in plants from tyrosine and phenylalanine via the sequential reaction of phenylalanine ammonia-lyase (PAL), cinnamate-4-hydroxylase (C4H), 4-coumarate:coenzyme A ligase (4CL) and chalcone synthase (CHS). Chalcones are converted into the corresponding flavanones by the action of chalcone isomerase (CHI), or non-enzymatically under alkaline conditions. PAL from the yeast Rhodotorula rubra, 4CL from an actinomycete Streptomyces coelicolor A3(2), and CHS from a licorice plant Glycyrrhiza echinata, assembled as artificial gene clusters in different organizations, were used for fermentation production of flavanones in Escherichia coli. Because the bacterial 4CL enzyme attaches CoA to both cinnamic acid and 4-coumaric acid, the designed biosynthetic pathway bypassed the C4H step. E. coli carrying one of the designed gene clusters produced about 450 microg naringenin/l from tyrosine and 750 microg pinocembrin/l from phenylalanine. The successful production of plant-specific flavanones in bacteria demonstrates the usefulness of combinatorial biosynthesis approaches not only for the production of various compounds of plant and animal origin but also for the construction of libraries of "unnatural" natural compounds.

Production of plant-specific flavanones by Escherichia coli containing an artificial gene cluster.

In plants, chalcones are precursors for a large number of flavonoid-derived plant natural products and are converted to flavanones by chalcone isomerase or nonenzymatically. Chalcones are synthesized from tyrosine and phenylalanine via the phenylpropanoid pathway involving phenylalanine ammonia lyase (PAL), cinnamate-4-hydroxylase (C4H), 4-coumarate:coenzyme A ligase (4CL), and chalcone synthase (CHS). For the purpose of production of flavanones in Escherichia coli, three sets of an artificial gene cluster which contained three genes of heterologous origins--PAL from the yeast Rhodotorula rubra, 4CL from the actinomycete Streptomyces coelicolor A3(2), and CHS from the licorice plant Glycyrrhiza echinata--were constructed. The constructions of the three sets were done as follows: (i) PAL, 4CL, and CHS were placed in that order under the control of the T7 promoter (P(T7)) and the ribosome-binding sequence (RBS) in the pET vector, where the initiation codons of 4CL and CHS were overlapped with the termination codons of the preceding genes; (ii) the three genes were transcribed by a single P(T7) in front of PAL, and each of the three contained the RBS at appropriate positions; and (iii) all three genes contained both P(T7) and the RBS. These pathways bypassed C4H, a cytochrome P-450 hydroxylase, because the bacterial 4CL enzyme ligated coenzyme A to both cinnamic acid and 4-coumaric acid. E. coli cells containing the gene clusters produced two flavanones, pinocembrin from phenylalanine and naringenin from tyrosine, in addition to their precursors, cinnamic acid and 4-coumaric acid. Of the three sets, the third gene cluster conferred on the host the highest ability to produce the flavanones. This is a new metabolic engineering technique for the production in bacteria of a variety of compounds of plant and animal origin.

The Effect of Cytochrome Oxidase Inhibitors on the Thermotolerance of Yeasts

The investigation of the effect of the cytochrome oxidase inhibitors sodium cyanide and sodium azide on the thermotolerance of the yeasts Rhodotorula rubra, Debaryomyces vanriji, and Saccharomyces cerevisiae showed that these inhibitors diminish the thermotolerance of R. rubraand D. vanriji, but do not affect the thermotolerance of S. cerevisiae. Taking into account the fact that, unlike the latter yeast, R. rubra and D. vanriji are nonfermentative yeasts, the difference in the effects of the inhibitors on the yeast thermotolerance can be readily explained by the different types of glucose utilization (either oxidative or fermentative) in these yeasts. The data obtained also provide evidence that there is a correlation between the functional activity of mitochondria and the thermotolerance of yeast cells.

The absence of direct relationship between the ability of yeasts to grow at elevated temperatures and their survival after lethal heat shock

The study of the growth of the yeasts Rhodotorula rubra, Saccharomyces cerevisiae, and Debaryomyces vanriji at elevated temperatures and their survival after transient lethal heat shock showed that the ability of these yeasts to grow at supraoptimal temperatures (i.e., their thermoresistance) and their ability to tolerate lethal heat shocks (i.e., their thermotolerance) are determined by different mechanisms. The thermotolerance of the yeasts is suggested to be mainly determined by the division rate of cells before their exposure to heat shock.

A new isolation method for labyrinthulids using a bacterium, Psychrobacter phenylpyruvicus.

A new isolation method for labyrinthulids, marine microbes with spindle-shaped vegetative cells and gliding movement, is presented. The method for isolating labyrinthulids has been found to be more difficult and less reproducible than that for thraustochytrids, classified in the same order. So far serum seawater agar fortified with antibiotics has been proposed to be the best for isolation of labyrinthulids. The method presented here involves placing plant samples on an agar medium on which a marine bacterium, Psychrobacter phenylpyruvicus, has been grown. The new method, which utilizes fallen mangrove leaves as source material, was more than twice as effective as isolation agar medium without the bacterium. The increased effectiveness appears to derive partly from the bacterial colonies' delaying extension of fungal mycelium. The bacterium was more effective for the isolation of labyrinthulids than either the bacterium Shewanella sp. or the yeast Rhodotorula rubra.