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Anaerobic Fungi: Past, Present, and Future Edited By: Robert Czajkowski, Matthias Hess1*†#, Shyam S

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Anaerobic Fungi: Past, Present, and Future Edited By: Robert Czajkowski, Matthias Hess1*†#, Shyam S fmicb-11-584893 October 15, 2020 Time: 17:12 # 1 REVIEW published: 21 October 2020 doi: 10.3389/fmicb.2020.584893 Anaerobic Fungi: Past, Present, and Future Edited by: Robert Czajkowski, Matthias Hess1*†#, Shyam S. Paul2#, Anil K. Puniya3#, Mark van der Giezen4#, University of Gdansk,´ Poland Claire Shaw1#, Joan E. Edwards5‡# and Katerinaˇ Fliegerová6†# Reviewed by: 1 Mostafa S. Elshahed, Systems Microbiology & Natural Product Discovery Laboratory, Department of Animal Science, University of California, 2 Oklahoma State University, Davis, Davis, CA, United States, Gut Microbiome Lab, ICAR-Directorate of Poultry Research, Indian Council of Agricultural 3 United States Research, Hyderabad, India, Anaerobic Microbiology Lab, ICAR-National Dairy Research Institute, Dairy Microbiology 4 Birbal Singh, Division, ICAR-National Dairy Research Institute, Karnal, India, Department of Chemistry, Bioscience and Environmental 5 Indian Veterinary Research Institute Engineering, University of Stavanger, Stavanger, Norway, Laboratory of Microbiology, Wageningen University & Research, 6 (IVRI), India Wageningen, Netherlands, Laboratory of Anaerobic Microbiology, Institute of Animal Physiology and Genetics, Czech Academy of Sciences, Prague, Czechia *Correspondence: Matthias Hess [email protected] Anaerobic fungi (AF) play an essential role in feed conversion due to their potent fiber †These authors have contributed degrading enzymes and invasive growth. Much has been learned about this unusual equally to this work fungal phylum since the paradigm shifting work of Colin Orpin in the 1970s, when he #ORCID: Matthias Hess characterized the first AF. Molecular approaches targeting specific phylogenetic marker orcid.org/0000-0003-0321-0380 genes have facilitated taxonomic classification of AF, which had been previously been Shyam S. Paul complicated by the complex life cycles and associated morphologies. Although we now orcid.org/0000-0002-9549-5741 Anil K. Puniya have a much better understanding of their diversity, it is believed that there are still orcid.org/0000-0003-0043-5330 numerous genera of AF that remain to be described in gut ecosystems. Recent marker- Mark van der Giezen orcid.org/0000-0002-1033-1335 gene based studies have shown that fungal diversity in the herbivore gut is much like Claire Shaw the bacterial population, driven by host phylogeny, host genetics and diet. Since AF are orcid.org/0000-0002-2495-0612 major contributors to the degradation of plant material ingested by the host animal, it is Joan E. Edwards orcid.org/0000-0003-0759-633X understandable that there has been great interest in exploring the enzymatic repertoire of Katerinaˇ Fliegerová these microorganisms in order to establish a better understanding of how AF, and their orcid.org/0000-0001-9439-8168 enzymes, can be used to improve host health and performance, while simultaneously ‡ Present address: Joan E. Edwards, reducing the ecological footprint of the livestock industry. A detailed understanding of Palital Feed Additives, AF and their interaction with other gut microbes as well as the host animal is essential, Velddriel, especially when production of affordable high-quality protein and other animal-based Netherlands products needs to meet the demands of an increasing human population. Such a Specialty section: mechanistic understanding, leading to more sustainable livestock practices, will be This article was submitted to possible with recently developed -omics technologies that have already provided first Microbial Symbioses, a section of the journal insights into the different contributions of the fungal and bacterial population in the rumen Frontiers in Microbiology during plant cell wall hydrolysis. Received: 18 July 2020 Accepted: 29 September 2020 Keywords: anaerobic digestion, carbohydrate-active enzymes, food security, herbivores, methanogenesis, Published: 21 October 2020 Neocallimastigomycota, rumen, sustainable agriculture Citation: Hess M, Paul SS, Puniya AK, INTRODUCTION van der Giezen M, Shaw C, Edwards JE and Fliegerová K (2020) Anaerobic Fungi: Past, Present, The ability of herbivorous animals to ferment recalcitrant plant fiber into utilizable forms of and Future. energy, most cases in the form of volatile fatty acids (VFAs), has been attributed to the trillions Front. Microbiol. 11:584893. of microbial cells that inhabit their gastrointestinal tract (Dearing and Kohl, 2017). Importantly, doi: 10.3389/fmicb.2020.584893 energy stored within complex plant carbohydrates is made accessible to the host animal Frontiers in Microbiology| www.frontiersin.org 1 October 2020| Volume 11| Article 584893 fmicb-11-584893 October 15, 2020 Time: 17:12 # 2 Hess et al. Anaerobic Fungi in Herbivores only through the synergistic activity of its gut microbes to improve the feed conversion efficiency of plant-based animal (Morais and Mizrahi, 2019). feeds. In this review, we discuss the current understanding of AF Independent of which type of mammalian herbivore digestive biology, ecology and their role in livestock production, along with physiology is considered, all mammalian herbivores have future perspectives on how their true value can be realized. evolved specialized gut compartments to give home to a complex microbial ecosystem of bacteria, anaerobic fungi (AF), protozoa, methanogenic archaea and bacteriophages (Morgavi TAXONOMY et al., 2013). All three of the major types of herbivorous mammals depend on these microbiomes and their proper Anaerobic fungi were first documented over 100 years ago, function to support their health and performance: ruminants when their flagellated zoospores were mistakenly identified (e.g., cattle, goats, and sheep), pseudoruminants (e.g., camelids as flagellate protozoa (Liebetanz, 1910; Braune, 1913). After and hippopotami) and hindgut herbivores (e.g., elephants, first being incorrectly classified as Protozoa (Liebetanz, 1910; donkeys, horses and zebras). Furthermore, in foregut fermenting Braune, 1913), they were reclassified, due to the significant ruminants and pseudoruminants the forestomach microbes evidence collected over many years by Orpin, as belonging themselves also serve as a substantial source of protein and to the fungal phylum Chytridiomycetes (Barr, 1980, 1988). vitamins for the host unlike in hindgut herbivores (Mizrahi, In 2007, they were acknowledged as being a distinct phylum, 2013; Nagaraja, 2016). An excellent review of herbivore the Neocallimastigomycota (Hibbett et al., 2007). Recently, gastrointestinal physiology, including detailed drawings, and Tedersoo et al.(2018) proposed a new fungal subkingdom, its role on microbial fermentation of plant biomass was Chytridiomycota, grouping the Neocallimastigomycota summarized by Dehority(2002). with two additional phyla, the aerobic Chytridiomycota and Foregut fermenters are capable of an enhanced degradation Monoblepharomycota, thereby acknowledging the monophyletic of plant biomass that is facilitated by a prolonged (60–90 h) origin of the zoosporic chitinous fungi (Ebersberger et al., 2012). retention time of the feed material in the rumen, the first and The Neocallimastigomycota contains only one order largest of three pre-gastric chambers of the foregut fermenter (Neocallimastigales) and one family (Neocallimastigaceae) digestive tract. Gastric digestion in the ruminant digestive system comprising eighteen genera; namely the monocentric rhizoidal occurs in the abomasum, which is the fourth chamber of the Neocallimastix, Piromyces, Oontomyces, Buwchfawromyces, ruminant’s foregut. Plant material in the cecum and colon of Pecoramyces, Liebetanzomyces, Feramyces, Agriosomyces, a hindgut fermenter, on the other hand, is retained on average Aklioshbomyces, Capellomyces, Ghazallomyces, Joblinomyces, only half as long (i.e., 30–40 h in equines) as it is in the Khoyollomyces, and Tahromyces; the polycentric rhizoidal ruminant’s digestive tract and is consequently less completely Anaeromyces and Orpinomyces; and the bulbous Caecomyces and digested (Trinci et al., 1994). Cyllamyces. Key morphological features of AF taxa, such as the Despite the recent significant advances in our understanding number of flagella on zoospores, type of thallus and rhizoids, of how bacteria and archaea influence the function, resilience, steps of zoosporangial development, and the shape of sporangia, and the environmental footprint of herbivorous mammals such are listed in Table 1. as ruminants (Kittelmann et al., 2014; Henderson et al., 2015; Liu Although morphological features have been crucial for the et al., 2017; Huws et al., 2018; Wallace et al., 2019), our knowledge classification of AF in the past, this approach is encumbered of AF and their influence on the host animal remains limited. with difficulties due to the extensive morphological variations, This limited knowledge is perhaps not surprising considering pleomorphism in sporangial and rhizoidal structures, similarities that until the mid-20th century it was still believed that all in morphological features of monocentric/uniflagellate genera, fungi required oxygen (Trinci et al., 1994). It was only in 1975 failure to produce sporangia, and the absence of zoosporogenesis that the ground-breaking work of Colin Orpin unequivocally in some polycentric species. Hence, ribosomal RNA (rRNA) confirmed the existence of AF, changing the accepted dogma of operon-based analysis is also needed to verify and support the time. Shortly after AF were first isolated and described in classification of AF. The topology of the ribosomal RNA (rrn) the rumen (Orpin,
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