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Systematic Review of Publicly Available Non-Dikarya Fungal Proteomes For Sista Kameshwar and Qin Bioresour. Bioprocess. (2019) 6:30 https://doi.org/10.1186/s40643-019-0264-6 REVIEW Open Access Systematic review of publicly available non-Dikarya fungal proteomes for understanding their plant biomass-degrading and bioremediation potentials Ayyappa Kumar Sista Kameshwar and Wensheng Qin* Abstract In the last two decades, studies on plant biomass-degrading fungi have remarkably increased to understand and reveal the underlying molecular mechanisms responsible for their life cycle and wood-decaying abilities. Most of the plant biomass-degrading fungi reported till date belong to basidiomycota or ascomycota phyla. Thus, very few studies were conducted on fungi belonging to other divisions. Recent sequencing studies have revealed complete genomic sequences of various fungi. Our present study is focused on understanding the plant biomass-degrading potentials, by retrieving genome-wide annotations of 56 published fungi belonging to Glomeromycota, Mucoromycota, Zoopago- mycota, Blastocladiomycota, Chytridiomycota, Neocallimastigomycota, Microsporidia and Cryptomycota from JGI-Myco- Cosm repository. We have compared and analyzed the proteomic annotations, especially CAZy, KOG, KEGG and SM clusters by separating the proteomic annotations into lignin-, cellulose-, hemicellulose-, pectin-degrading enzymes and also highlighted the KEGG, KOG molecular mechanisms responsible for the metabolism of carbohydrates (lignocellulolytic pathways of fungi), complex organic pollutants, xenobiotic compounds, biosynthesis of second- ary metabolites. However, we strongly agree that studying genome-wide distributions of fungal CAZyme does not completely corresponds to its biomass-degrading ability. Thus, our present study can be used as preliminary materi- als for selecting ideal fungal candidate for the degradation and conversion of plant biomass components, especially carbohydrates to bioethanol and other commercially valuable products. Keywords: Plant biomass, Lignocellulose, Bioremediation, Carbohydrate active enzymes (CAZymes), Eukaryotic orthologous groups (KOG), KEGG pathways Background oxygen, carbondioxide, solar luminosity (Baldauf and Early taxonomists classifed fungi under the plant king- Palmer 1993; Bruns 2006) (Fig. 1a). Although early evo- dom based on their lifestyle. However, with the devel- lutionary studies have reported that fungi have evolved opment of advanced molecular and phylogenetic from a common ancestor with that of unicellular fagel- techniques fungi were given a kingdom status. Evolu- lated aquatic organisms. However, there is no accepted tionary studies have reported that fungi have evolved in phylogenetic theory which explains about the evolution the early Neoproterozoic era followed by evolution over of the early fungi (James et al. 2000, 2006a; Karol et al. the period of time due to the earthly impacts including 2001; Tanabe et al. 2004). Previous studies have reported that chytridiomycota (fagellated cells) are group of true *Correspondence: [email protected] fungi which are phylogenetically connected to the sister Department of Biology, Lakehead University, 955 Oliver Road, Thunder groups mucoromycota, zoopagomycota, glomeromycota, Bay, Thunder Bay, ON P7B 5E1, Canada ascomycota and basidiomycota which have experienced © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Sista Kameshwar and Qin Bioresour. Bioprocess. (2019) 6:30 Page 2 of 19 Fig. 1 a Pictorial illustration of fungal evolution since the early Neoproterozoic era and the infuence of solar luminosity, carbon dioxide, oxygen, earth impacts over the geological timescale of fungal evolution (Hedges and Kumar 2009; Hedges et al. 2015), b hierarchical illustration of fungal phylogenetic classifcation an evolutionary loss of the fagellum (James et al. 2000, the terrestrial habitat by developing a flamentous growth 2006a; Karol et al. 2001; Tanabe et al. 2004). However, and aerially dispersed spores. Studies have reported that these non-fagellated fungi have evolutionarily adapted to early fungal phylogeny and fungal tree of life remained Sista Kameshwar and Qin Bioresour. Bioprocess. (2019) 6:30 Page 3 of 19 unresolved; however, in the recent years, phylogenetic for its plant cell wall (lignocellulose)-degrading abili- studies have questioned the phylogenetic lineage of the ties (Kameshwar and Qin 2016a). In our previous study, chytridiomycota, mucoromycota and zoopagomycota we have performed a large-scale comparative analysis of which resolved the phylogenetic aspects of these basal 42 wood rotting fungi representing white rot, brown rot groups with their relationships with ascomycota and and soft rot fungi (Sista Kameshwar and Qin 2017). Tis basidiomycota (James et al. 2000, 2006a; Karol et al. 2001; study has majorly reported that white rot fungi tenta- Tanabe et al. 2004) (Fig. 1b). Studies have classifed king- tively exhibit highest lignocellulolytic and soft rot fungi dom fungi into six true phyla: chytridiomycota, zygomy- tentatively exhibit highest cellulolytic and hemicellulo- cota, ascomycota, basidiomycota, glomeromycota and lytic potentials (Sista Kameshwar and Qin 2017). deuteromycota (McLaughlin et al. 2001; Silar 2016). How- Te arbuscular mycorrhizal (AM) fungi belonging to ever, the recent higher level phylogenetic studies classi- the glomeromycota phyla play a crucial role both eco- fed fungi into: Dikarya (ascomycota, basidiomycota), logically and environmentally (Morton and Benny 1990). glomeromycota, chytridiomycota, neocallimastigomycota, AM fungi are asexual organisms and obligate symbiotes blastocladiomycota, kickxellomycota, microsporidia and of vascular plants (as AM fungi penetrate the plant sub- cryptomycota, respectively (Hibbett et al. 2007) (Fig. 1a). strate using its mycelium). Studies have reported that Advancement of molecular techniques 18srRNA and plants depend on the symbiotic mycorrhizae rather than whole-genome sequencing techniques are currently the roots for the uptake of phosphate ion from the soil being used to understand and reveal the phylogenetic (Morton and Benny 1990; Schüßler et al. 2001b; Smith relationships among the fungi. Development of advanced and Read 1997). Tus, plants obtain inorganic micro- genome sequencing techniques and online genomic nutrients with the aid of AM fungi and in return fungi repositories have enhanced the current days knowledge obtains carbohydrates from plant, this exchange hap- of fungal lifestyle and evolution. Te fungal genomic pens through the intracellular symbiotic interfaces. Te repositories such as joint genome institute MycoCosm molecular evolutionary techniques such as small subunit (Grigoriev et al. 2011; Nordberg et al. 2013), 1000 fun- rRNA sequences report that they share a common ances- gal genome project and Hungate collection residing in tor route with Dikarya and the present glomeromycota the rumen microbial genomics network are continu- consists four orders: (a) diversisporales, (b) glomerales, ously enhancing the genomic details of various fungi. (c) archaeosporales and (d) paraglomerales (Redecker Studies being conducted to understand the genomic et al. 2013; Schüßler et al. 2001a, b). Till date, studies potentials of diferent fungi belonging to diferent phyla have reported approximately 300 glomeromycota species were compared for their plant cell wall-degrading poten- based on their spore morphology (Chen et al. 2018). tials to explore their applications in biofuel and biore- Zygomycota are considered as true fungi and contain mediation industries (Kameshwar and Qin 2018; King chitin in their cell walls. Tese fungi were found to be et al. 2011; Rytioja et al. 2014; Sista Kameshwar and Qin emerged from the other fungi approximately 600 to 1400 2017; Zhao et al. 2013). Till date, there are 1054 whole- million years ago (Berbee and Taylor 2001a, b, Heck- genome sequences of fungi belonging to diferent phyla man et al. 2001). Tese terrestrial fungi live in decay- in JGI-MycoCosm repository, out of which 444 whole- ing plants or animals and soil material, and some fungal genome sequences of fungi have been published and species are parasites of plants, insects, while some spe- publicly available and the remaining 610 whole-genome cies are in symbiotic relationships with the plants (Raven sequences of fungi were under study and unpublished et al. 2005). Zygomycetes fungi are flamentous, non- (Grigoriev et al. 2011; Nordberg et al. 2013). fagellated, and importantly they form zygospores with Fungi belonging to the ascomycota and basidiomycota in the zygosporangium formed as a result of sexual cycle. phyla were highly studied compared to other phyla. Till Major transition from the earliest diverging zoosporic date, approximately 349 basidiomycetous and 588 asco- fungi led to the phyla cryptomycota, chytridiomycota, mycetous fungi whole-genome sequencing studies were neocallimastigomycota, blastocladiomycota and resulted reported in public repositories. During the process of towards the rise of non-fagellated flamentous multi- evolution, fungi have developed as bio-decomposers/ cellular Dikaryan fungi (Spatafora et al. 2016). Studies decayers of the organic material. In nature, fungi
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