Microparticles on Fungal Fermentation

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1		Ali Demirci	--	2532	2022-12-21 04:31:53	\|
2	update references and layout	Rita Xu	-3 word(s)	2529	2022-12-21 07:39:45	\|

This entry is adapted from the peer-reviewed paper 10.3390/pr10122681

Ranging from simple food ingredients to complex pharmaceuticals, value-added products via microbial fermentation have many advantages over their chemically synthesized alternatives. Some of such advantages are environment-friendly production pathways, more specificity in the case of enzymes as compared to the chemical catalysts and reduction of harmful chemicals, such as heavy metals or strong acids and bases. Fungal fermentation systems include yeast and filamentous fungal cells based on cell morphology and culture conditions.

filamentous fungal fermentation microparticles microparticle-enhanced cultivation

1. Introduction

Fermentation has always been a crucial part of human civilizations even before the extensive knowledge of microbiology and industrial biotechnology. Ancient humans used to make bread, beer, and many other fermentation-based products without the knowledge of underlying microbiological principles ^[1]. Records of bread and alcoholic beverage making can be traced back to the Egyptians (5000 BC) and Babylonians (6000 BC) ^[2]. At the end of the nineteenth and start of the twentieth century, the enhanced knowledge of microbiology helped in the development of more sophisticated fermentation-based products. The microorganisms varied from simple prokaryotic bacteria to mycelial-forming eukaryotic fungi. Each microorganism is known for specific fermented products and commodities that make it an industrial producer of that product. Among these microorganisms, fungi are known for many products, including bread, alcoholic beverages, pharmaceuticals, vitamins, food additives, biofuels, enzymes, organic acids, fatty acids, and sterols ^[3]. The use of fungi as fermentation producers has increased significantly over the last decades ^[4]. Currently, only the plant biomass-hydrolyzing fungal enzyme industry is worth $4.5 billion market and is expected to increase to $9.74 billion by 2026 ^[1].

There are many different types of fungi including, yeasts, mushrooms, and filamentous fungi or molds. Each differs in terms of its cell structure, growth patterns, and generation time ^[2]. All fungi are, however, eukaryotic cells, which makes them different from bacteria ^[3]. Filamentous fungi are gaining attention due to the robust production of bioenergy-related enzymes, such as cellulases and hemicellulases ^[5]. There has been greater research interest in developing mechanisms for the industrial fermentation of filamentous fungi to produce a diverse range of products with general categories of food-related items, alcoholic beverages, juice, pulp, bioenergy, and detergent industries. There are many kinds of filamentous fungal genera that have gained attention in their production of a specific or diverse range of products. Some examples include Aspergillus, Trichoderma, Penicillium, and Acremonium species, among many others.

There are mainly two microbial fermentation system types: solid-state and submerged fermentations. In solid-state fermentation, the microorganisms have limited moisture content and are cultivated on a solid substrate. In submerged fermentation, on the other hand, the microbial media is in a liquid state with freely available nutrients to all microbial cells. Solid-state fermentation is usually used for mold, while submerged is used for bacteria and yeast cultures. Regardless of the fermentation type, every fermentation product and microorganism requires specific culture conditions with upstream and downstream processing techniques. For example, in the case of yeast cells, which are freely suspended in the media, the use of spargers or propellers is efficient in the distribution of nutrients and oxygen in the bioreactor. However, the same type of instrument can disrupt the mycelium in the filamentous fungal bioreactor, which consists of heavy mycelial clumps or pellets and can result in the premature death of the fungal cells and their inability to produce the required product ^[2]. Therefore, airlift or bubble column reactors are used for such types of fermentation ^[2]. The main challenge in submerged fungal fermentation is the formation of mycelial clumps or pellets, which disrupts the even distribution of oxygen and nutrients.

The mycelial growth of filamentous fungi under submerged conditions can occur in many forms. The basic vegetative form is like a tubular filament and is known as a hypha. The hypha is formed through the germination of a single reproductive spore. The growth and spreading of a hypha into branches results in the formation of a complex structure known as mycelium. When grown in a free liquid phase or submerged conditions, these mycelial structures can take many different forms based on genetics, inoculum properties, and culture conditions ^[6]. The mycelium can either disperse into loosely branched structures or can aggregate into dense clumps or pellets ^[4]. The same fungal species can form two different forms of mycelial structures based on the culture conditions and product. For example, in the case of Aspergillus niger, pectic enzyme production culture conditions produce filamentous growth, while pellets are produced under the fermentation conditions for citric acid ^[4]. Another example is Penicillium chrysogenum, for which the pelleted form is preferred in the production of penicillin while it shows other morphological forms as well. After the initial stationary and early growth phases, the production of mycelial clumps and pellets becomes problematic as the viscosity of the medium increases with the growing mycelial mass ^[4]. Therefore, many strategies have been developed to control the physiology of fungal cells under submerged fermentation conditions.

One strategy that has recently gained attention to control fungal physiology under submerged conditions is the use of microparticles. Microparticles are inert particles of various sizes that can affect the morphology of the microbial cells in fermentation without chemically interacting with the media or the microbial cells. Many types of microparticles have been studied recently for their effect on fungal morphology and the production of various fermentation-based products ^[7]^[8]^[9]. There are many hypotheses as to why the addition of a low concentration of microparticles changes fungal morphology and productivity under different submerged conditions. One hypothesis is that microparticles affect the size of the mycelial clumps or pellets, thus facilitating the oxygen transfer to the fungal cells ^[10]. Another one is that it affects the interaction between fungal hyphae. The main advantage of using microparticles is their ease of application. The addition of microparticles after preparing the microbial media is straightforward. After the fermentation stages, the microparticles can be filtered out from the broth along with the fungal biomass. They can also be separated from the biomass using centrifugation and washing, although this technique has not been reported in the literature so far. The separated microparticles can be recycled for the next fermentation batch. Currently, the most prominent type of research on microparticles in fungal fermentation is their effect on yield, fungal physiology and overall changes in the fermentation run. However, more research is needed to see if such particles can be washed out of the broth for the next fermentation cycle.

2. Advantages and Disadvantages of Fungal Fermentation

Just like any other microbial fermentation, fungal fermentation requires specific requirements, including inoculum size, aeration, agitation, and nutrient composition. Fungal fermentations can be of many kinds based on the type of fungi. The yeast fermentation can be easily controlled as compared to the filamentous fungal fermentation because of their differences in the cell structure and formation. The yeast fermentation is mostly done in submerged fermentation. Filamentous fungal fermentation, which is a promising technique for various enzymes and other value-added products, is predominantly solid-state fermentation. However, solid-state fermentation, on the other hand, has many disadvantages, ranging from the difficulty in obtaining the even distribution of nutrients to the problems in scale-up ^[11]. Therefore, submerged fungal fermentation has been researched extensively for filamentous fungal species such as Aspergillus niger, Trichoderma reesei, and many others.

There are many advantages of filamentous fungal fermentation as compared to yeast or bacterial fermentation. The most prominent advantage is the diverse range of proteins, enzymes, and many secondary metabolites that are produced by filamentous fungal species and are not produced by other microbial species ^[1]^[12]. Another advantage is the higher enzyme titers as compared with other microbial enzymes ^[13]. In addition, bacterial cells require a more sophisticated nutrient composition as compared with fungal cells. The bacteria and yeast prefer simple carbon sources such as glucose or other mono and disaccharides. On the other hand, there are many fungal species that can thrive on complex and diverse carbon sources such as cellulose, hemicellulose, and pectin ^[14]^[15]. There are many studies that have been conducted to show the effectiveness of complex and unconventional carbon sources that can be used to produce value-added products by using fungal fermentation. Table 1 shows some of such studies in the literature.

Table 1. Examples of complex carbon sources for the production of value-added products from fungal fermentation systems.

Carbon Source	Fungal Strain(S)	Value-Added Products	References
Spent hydrolysates	Trichoderma reesei Rut C-30	Enzymes	^[15]
Mixture of dry leaves	Aspergillus niger	Cellulase	^[16]
Aguamiel	Aspergillus niger GH1, Aspergillus niger PSH and Aspergillus oryzae DIA-MF	Fructooligosaccharides (FOS)	^[17]
Whole maize flour	Aspergillus niger	Citric acid	^[18]
Corn cob and sawdust	Aspergillus niger	Xylanase	^[19]
Corn cobs	Aspergillus flavus AW1	Xylanase	^[20]
Sorghum xylans	Aspergillus fumigatus RSP-8	Xylanase	^[21]
Algerian date varieties	Aspergillus niger ATCC 16888	Citric acid	^[22]
Rice husk, cottonseed cake, and red gram husk	Aspergillus niger MTCC 872	Lipases	^[23]
Distillers dried grains with solubles (DDGS)	Aspergillus niger (NRRL 330) and (NRRL 567)	Cellulases and hemicellulases	^[24]
Sunflower stalks	Aspergillus sp.	Xylanase	^[25]
Sugarcane bagasse	Mucor circinelloides	Single cell oil	^[26]
Babassu cake	Penicillium simplicissimum	Lipase	^[27]
Agro-industrial bioproducts	Moniliella SB9 and Penicillium sp. EGC5	Polygalcturonase and pectin lyase	^[28]
Sweet potato extract	Gongronella butleri USDB 0201	Chitosan	^[29]
Wheat and soybean bran	Aspergillus niger and Aspergillus flavus	Lipase	^[30]
Textile waste	Trichoderma reesei ATCC 24449	Cellulase	^[31]
Waste streams from ethanol and bread	Neurospora intermedia	Ethanol, biomass and a feed product	^[32]

The main disadvantage of filamentous fungal fermentation, as compared with yeast and bacterial fermentation, is the undesirable production of complex mycelial structures, such as fungal pellets that make the even distribution of oxygen and nutrients difficult in submerged fermentation. Therefore, solid-state fermentation is mostly preferred over submerged fermentation for filamentous fungi. However, the build-up of temperature, oxygen, pH, and moisture gradient makes the scaling-up of solid-state fermentation very challenging ^[11]. Therefore, there is a pressing need for the development of submerged fermentation techniques that can help in the cultivation of filamentous fungal strains under submerged fermentation. The productivity and yield are also lower under submerged conditions as compared to solid-state fermentation. The main reason is the substrate inhibition at higher sugar levels in liquid suspended-cell fermentation ^[33]. There have been many approaches proposed in the recent literature to overcome such problems. The most prominent strategy is the optimization of aeration and agitation to control the size of the mycelial clumps. However, a recent development is the use of microparticles to control the fungal morphology and to release the product more efficiently into the liquid phase ^[34].

3. Fungal Cell Growth Characteristics (Morphology) and Effects on the Product Formation

Fungal microorganisms, widely used in biotechnological processes, exhibit different complex morphological forms, such as mycelium, clumps, and pellets ^[34]. These forms could vary accordingly, due to features of submerged cultures, and process performance in a bioreactor is directly affected by morphological varieties ^[35]. Morphology affects the yield of upstream and downstream processes. The fermentation conditions, such as the rheology of broth, mass, and oxygen transfer rate, are varied depending on the morphology. Accordingly, productivity is affected by the alteration of these conditions. Furthermore, biomass formation affects purification steps. Compact biomass formation can be easily removed from fermentation broth by comparison hyphal formation ^[36].

The production of various fungal products, which are target products or second metabolites, could differ based on the morphological characteristics of fungal microorganisms. For example, the production yield of the other metabolites is generally higher in pellet forms, or mycelia forms are effective fungal microorganisms for enzyme production ^[36]. Although there are some approaches like these in the literature, choosing a convenient morphological form, such as mycelial or pellet, is one of the most important challenges for production in optimum yield. The viscosity of broth increases as mycelium forms and the flow behavior of broth turns into pseudoplastic ^[37]. Similarly, mass transfer rates, particularly gas-liquid oxygen transfer, are negatively affected. Moreover, higher oxygen input and agitation rate are required for production at the desired levels ^[4]. On the other hand, the pelleted growth form does not have as strong an impact as mycelium on viscosity. However, there are a few disadvantages that originate from the nature of pellet form morphology. During the fermentation process, biomass density increases and larger non-homogeneous pellet structures, which have less porosity, begin to form. Under these conditions, lower nutrient uptake occurs with the effect of an intense hyphal network, and lack of substrate has an impact on metabolism and leads to autolysis in the central part of pellet, eventually. The constitution of smaller pellet forms are generally desirable for fungal fermentations to avoid nutrient limitation and autolysis ^[35]^[38]. Therefore, many of the research studies in the literature indicated that the product yield can be improved by controlling the morphology of fungal microorganisms with different strategies.

4. Conventional Methods for Controlling Fungal Cell Growth in Liquid Fermentation

Various conventional techniques were developed and used in fungal submerged fermentation to overcome these limitations, which are derived from the morphological properties of fungi. These techniques, also known as morphology engineering, focus generally on modifying the environmental conditions of fermentations to improve productivity. There is plenty of research in the literature about various factors which affect morphology in different fermentations type. These factors, known as environmental inputs, are temperature, pH, dissolved oxygen concentration, agitation, impeller type, reactor type, and media composition. Some of the research on the effects of these inputs were summarized. In addition, some factors related with preferred fungi for production were also investigated, such as cultivation type, inoculum concentration, age of mycelium, and viability of spore ^[4]^[36]^[39].

The effects of inoculum on the morphology and yield were investigated in many research studies in the literature. For example, Liu et al. ^[40] demonstrated that the effects of inoculum on Rhizopus oryzae (NRRL 395) (ATCC 9363), R. oryzae (ATCC 20344), and R. oryzae (ATCC10260). They reported that the probability of forming pellets increased at high inoculum spore concentrations (up to 3 × 109 spores/L). In another study, when the initial spore concentrations of Aspergillus terreus (ATCC 20542) were below 2 × 109 spores/L, the biosynthesis of the second metabolite, such as geodin, was observed ^[41]. The correlation between pH and the aggregation of Aspergillus niger conidia were also investigated. It was demonstrated that the number of pellets was higher at pH 4.0 than at pH 7.0. In addition, productivity also decreased with increasing of at extreme pH values ^[42].

Apart from these approaches, inputs, such as agitation and aeration, were studied to define their impact on morphology and productivity. Chen et al. ^[43] reported that pellets were not formed when the agitation speed was 200 rpm, but L-malate production and A. oryzae pellets number were increased by increasing of agitation speed to 600 rpm. They also reported that, although the increasing aeration rate improved pellet number and product concentration initially, they decreased subsequently. It was determined that lower agitation speed and milder shear stress were improved pellet formation and enzyme production due to reducing of broth viscosity in fed-batch fermentation ^[44]. The effect of volumetric power input, which was controlled by different agitation speed and aeration rate, were investigated to improve of pellet morphology of Aspergillus niger (AB1.13) and glucoamylase productivity. Results indicated that pellet concentration and production of glucoamylase were increased with increasing of volumetric power input by aeration rate ^[45].

Most of the productivity problems that originated from the morphological properties of fungi can be overcome by using conventional methods at small scales. However, conventional methods have limited impact because of the high energy requirement and non-feasible large-scale applicability ^[36]^[39]. Therefore, they have been less efficient and preferable in comparison with new morphological engineering techniques as microparticles or genetical modifications.

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