Bacteriology & Mycology: Open Access

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Received: January 01, 1970 | Published: ,

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Abstract

Of the main types of microorganisms that inhabit the rumen, fungi remain the least characterized group. They have been found to be critical as primary colonizers and digesters of plant matter in the rumen. While they share common fungal characteristics, such as a chitin-containing cell wall, a multi-stage life cycle and arrays of potent carbohydrate-digesting enzymes, they have evolved to an anaerobic lifestyle through other adaptations, such as the hydrogenosome, an organelle which may have developed from mitochondria. Evidence based on comparative genomics is indicating that a number of these adaptations may have involved horizontal gene transfer with other groups of rumen microorganisms.

Keywords: rumen, anaerobic, fungi, hydrogenosome, lignocellulosic biomass

Introduction

Harvested as either prey or livestock, ruminants have played a critical role throughout human history,¹ and they are expected to remain essential in ensuring food security for a rapidly growing and urbanizing global population.² Like other herbivores, ruminants do not encode in their genome enzymes that are effective in breaking down plant fiber. To convert lignocellulosic biomass into utilizable energy, they rely on the metabolic activities of symbiotic microbial communities that reside in the rumen segment of their four-chambered stomach³. Ruminal microbial communities consist of complex and diverse assortments of bacterial, methanogenic, protozoal and fungal species, which, as a group, metabolize plant fiber polymers into short chain fatty acids (SCFAs) that are rapidly absorbed by the rumen epithelium.⁴ These rumen-produced SCFAs, a mixture composed primarily of acetate, propionate and butyrate, contribute up to 80% of the energy requirements of the ruminant host.⁵

Dating back to the work of Robert Hungate and other pioneers of rumen microbiology, decades of research efforts have provided great insights into this complex microbial ecosystem.⁶ In recent years, however, an increasing number of community-level analyses using DNA sequencing-based techniques have revealed that the complexity of the rumen microbial ecosystem is not only far greater than had been estimated by culturing-dependent techniques, but also that the vast majority of rumen microorganisms remain to be characterized. A factor likely to foster such high microbial diversity include the ruminant diet, which can support a wide array of metabolic specialists with overlapping functions.^7,8The difficulties experienced in trying to isolate additional rumen microbial species is the result of a number of factors, such as their anaerobic lifestyle and the intricate networks of mutually beneficial trophic relationships amongst members of the community that are required for them to achieve high levels of efficiency.⁹

Of the different types of microorganisms that inhabit the rumen, fungi represent the most poorly characterized group. Due to their low cellular density and the difficulties in identifying them,^10,11 rumen fungi were initially thought to have only a minimal involvement in ruminant digestion. However, increasing evidence is supporting their function as primary colonizers and digesters of plant matter in the rumen. Indeed, the presence of plant-based fibrous material in the rumen rapidly attracts zoospores, presumably through chemotaxis, which then proceed to colonize this substrate.¹²⁻¹⁴ Once attached, zoospores develop into mycelia, which then invade and break down plant fiber material. As a result of their activity and growth, rumen fungi are able to penetrate and disrupt plant tissue, which also increases the area of exposed substrate, facilitating access to other plant fiber utilizers such as bacteria and protozoa.

The important contribution of anaerobic fungi in ruminal digestion is also well supported by the observation that the rate at which they can metabolize plant matter is not affected by substrate particle size, while digestion rates for bacteria become reduced as the size of substrate particles increases. Anaerobic fungi are equipped with similar tools as their other relatives, breaking down lignocellulosic material by expressing a range of plant fiber metabolizing enzymes in addition to the invasive growth of their vegetative mycelium. Free as well as multi-enzyme complexes, such as cellulosomes, have been identified in rumen fungal species for which genome sequence is available.^15,16 However, as would be expected from their anaerobic lifestyle, rumen fungi are devoid of mitochondria, and do not possess cytochromes nor other biochemical components required for oxidative phosphorylation. Intriguingly, they use specific organelles, hydrogenosomes, to ferment monosaccharides released from the breakdown of plant structural polysaccharides into H₂, CO₂, formate and acetate as end products.^15,17 Since hydrogenosomes share common characteristics with mitochondria, they may have evolved from them.¹⁸⁻²⁰Rumen fungi are found in close association with methanogens, a mutually beneficial relationship in which the metabolic activity of the latter maintains H₂ at low levels which favors hydrogenase activity in the hydrogenosomes.²¹ While they can also produce lactate and ethanol as waste products, hydrogenosome-driven metabolism is likely more favorable.¹¹

While they share common fungal characteristics, such as a chitin-containing cell wall and a multi-stage life cycle,^10,22 rumen fungi appear to be phylogenetically distinct. Indeed, the genera so far identified cluster in a separate clade, which have been assigned to their own family (Neocallimastigaceae), order (Neocallimastigales), class (Neocallimastigomycetes), and phylum (Neocallimastigomycota).²³ They include three monocentric genera (Neocallimastix, Caecomyces and Piromyces) and three polycentric genera (Anaeromyces, Orpinomyces and Cyllamyces), with two additional proposed genera (Oontomyces and Buwchfawromyces) based on molecular data from other gut environments.^24,25 Comparative genomic studies have revealed that horizontal gene transfer appears to have played an important role in the adaptation of fungi to gut environments, which have included carbohydrate degrading enzymes as well as certain hydrogenosome enzymes.¹¹

Slowly, but surely, interest in anaerobic fungi has continued to gain in momentum, in large part driven by interest in their biotechnological potential.¹¹ With continued improvements in culturing, phylogenetic profiling, metagenomics, and gene annotation, more insights are likely yet to come for these fascinating fungi.