Filamentous fungi are critical to the decomposition of terrestrial organic matter and, consequently, in the global carbon cycle. In particular, their contribution to degradation of recalcitrant lignocellulose complexes has been widely studied. In this review, we focus on the functioning of terrestrial fungal decomposers and examine the factors that affect their activities and community dynamics. In relation to this, impacts of global warming and increased N deposition are discussed. We also address the contribution of fungal decomposer studies to the development of general community ecological concepts such as diversity–functioning relationships, succession, priority effects and home–field advantage. Finally, we indicate several research directions that will lead to a more complete understanding of the ecological roles of terrestrial decomposer fungi such as their importance in turnover of rhizodeposits, the consequences of interactions with other organisms and niche differentiation.

A thready affair: linking fungal diversity and community dynamics to terrestrial decomposition processes

While the natural niches of the soil bacterium Pseudomonas putida are unlikely to include significant amounts of free glycerol as a growth substrate, this bacterium is genetically equipped with the functions required for its metabolism. We have resorted to deep sequencing of the transcripts in glycerol-grown P. putida KT2440 cells to gain an insight into the biochemical and regulatory components involved in the shift between customary C sources (e.g. glucose or succinate) to the polyol. Transcriptomic results were contrasted with key enzymatic activities under the same culture conditions. Cognate expression profiles revealed that genes encoding enzymes of the Entner-Doudoroff route and other catabolic pathways, e.g. the gluconate and 2-ketogluconate loops, were significantly downregulated on glycerol. Yet, the compound simultaneously elicited a gluconeogenic response that indicated an efficient channelling of C skeletons back to biomass build-up through the glyoxylate shunt rather than energization of the cells through downwards pathways, i.e. tricarboxylic acid cycle and oxidative phosphorylation. The simultaneous glycolytic and gluconeogenic metabolic regimes on glycerol, paradoxical as they seem, make sense from an ecological point of view by favouring prevalence versus exploration. This metabolic situation was accompanied by a considerably low expression of stress markers as compared with other C sources.

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Metabolic and regulatory rearrangements underlying glycerol metabolism in Pseudomonas putida KT2440

Diatoms are prominent marine microalgae, interesting not only from an ecological point of view, but also for their possible use in biotechnology applications. They can be cultivated in phototrophic conditions, using sunlight as the sole energy source. Some diatoms, however, can also grow in a mixotrophic mode, wherein both light and external reduced carbon contribute to biomass accumulation. In this study, we investigated the consequences of mixotrophy on the growth and metabolism of the pennate diatom Phaeodactylum tricornutum , using glycerol as the source of reduced carbon. Transcriptomics, metabolomics, metabolic modelling and physiological data combine to indicate that glycerol affects the central-carbon, carbon-storage and lipid metabolism of the diatom. In particular, provision of glycerol mimics typical responses of nitrogen limitation on lipid metabolism at the level of triacylglycerol accumulation and fatty acid composition. The presence of glycerol, despite provoking features reminiscent of nutrient limitation, neither diminishes photosynthetic activity nor cell growth, revealing essential aspects of the metabolic flexibility of these microalgae and suggesting possible biotechnological applications of mixotrophy. This article is part of the themed issue ‘The peculiar carbon metabolism in diatoms9.

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Investigating mixotrophic metabolism in the model diatom Phaeodactylum tricornutum

The effective degradation of hazardous contaminants remains an intractable challenge in wastewater processing, especially for the high concentration of salty azo dye wastewater. However, some unique yeast symbionts identified from the termite gut system present an impressive function to deconstruct some aromatic compounds, which imply that they may be valued to work on the dye degradation for various textile effluents. In this investigation, a newly isolated and unique yeast strain, Sterigmatomyces halophilus SSA-1575, was identified from the gut system of a wood-feeding termite (WFT), Reticulitermes chinensis. Under the optimized ambient conditions, the yeast strain SSA-1575 showed a complete decolorization efficiency on Reactive Black 5 (RB5) within 24 h, where this azo dye solution had a concentration of a 50 mg/L RB5. NADH-dichlorophenol indophenol (NADH-DCIP) reductase and lignin peroxidase (LiP) were determined as the key reductase and oxidase of S. halophilus SSA-1575. Enhanced decolorization was recorded when the medium was supplemented with carbon and energy sources, including glucose, ammonium sulfate, and yeast extract. To understand a possible degradation pathway well, UV-Vis spectroscopy, FTIR and Mass Spectrometry analyses were employed to analyze the possible decolorization pathway by SSA-1575. Determination of relatively high NADH-DCIP reductase suggested that the asymmetric cleavage of RB5 azo bond was mainly catalyzed by NADH-DCIP reductase, and finally resulting in the formation of colorless aromatic amines devoid of any chromophores. The ecotoxicology assessment of RB5 after a decolorization processing by SSA-1575, was finally conducted to evaluate the safety of its metabolic intermediates from RB5. The results of Microtox assay indicate a capability of S. halophilus SSA-1575, in the detoxification of the toxic RB5 pollutant. This study revealed the effectiveness of halotolerant yeasts in the eco-friendly remediation of hazardous pollutants and dye wastewater processing for the textile industry.

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Performance of a Newly Isolated Salt-Tolerant Yeast Strain Sterigmatomyces halophilus SSA-1575 for Azo Dye Decolorization and Detoxification

Wallemia ichthyophaga is a fungus from the ancient basidiomycetous genus Wallemia (Wallemiales, Wallemiomycetes) that grows only at salinities between 10% (wt/vol) NaCl and saturated NaCl solution. This obligate halophily is unique among fungi. The main goal of this study was to determine the optimal salinity range for growth of the halophilic W. ichthyophaga and to unravel its osmoadaptation strategy. Our results showed that growth on solid growth media was extremely slow and resulted in small colonies. On the other hand, in the liquid batch cultures, the specific growth rates of W. ichthyophaga were higher, and the biomass production increased with increasing salinities. The optimum salinity range for growth of W. ichthyophaga was between 15 and 20% (wt/vol) NaCl. At 10% NaCl, the biomass production and the growth rate were by far the lowest among all tested salinities. Furthermore, the cell wall content in the dry biomass was extremely high at salinities above 10%. Our results also showed that glycerol was the major osmotically regulated solute, since its accumulation increased with salinity and was diminished by hypo-osmotic shock. Besides glycerol, smaller amounts of arabitol and trace amounts of mannitol were also detected. In addition, W. ichthyophaga maintained relatively small intracellular amounts of potassium and sodium at constant salinities, but during hyperosmotic shock, the amounts of both cations increased significantly. Given our results and the recent availability of the genome sequence, W. ichthyophaga should become well established as a novel model organism for studies of halophily in eukaryotes.

Osmoadaptation strategy of the most halophilic fungus, Wallemia ichthyophaga, growing optimally at salinities above 15% NaCl.

The growth and accumulation of intracellular polyols at reduced water activity (aw) were studied in 40 basidiomycetous yeast strains. The growth of most strains showed greater tolerance to NaCl than sorbitol at the same aw. No strain was able to grow below 0.90aw. 13C nuclear magnetic resonance spectroscopy revealed that glycerol was the major solute accumulated intracellularly by all the yeasts when grown to 0.96aw (NaCl). Arabitol or mannitol was also accumulated in some yeasts, whereas a few only accumulated glycerol. Analysis of six yeasts in detail revealed that the intracellular glycerol concentrations of five yeasts increased significantly when grown at 0.96aw (NaCl or sorbitol) compared with growth at 0.998aw. Arabitol and mannitol concentrations also increased, but not to the same degree. Intracellular potassium concentrations decreased when grown at 0.96aw (NaCl or sorbitol) and sodium increased, but only when grown at 0.96aw (NaCl). The survival of nine strains was evaluated in soil cultures and it was found that all grew at 100% field capacity, whereas at lower field capacity, only some strains grew or survived. The growth of basidiomycetous yeasts appears to be more sensitive to reduced aw than ascomycetous yeasts.

Obakeng M. Tekolo

Papers

The osmotic stress tolerance of basidiomycetous yeasts.