Horizontal gene transfer as an indispensable driver for Neocallimastigomycota evolution into a distinct gut-dwelling fungal lineage

Murphy, Chelsea L.; Youssef, Noha H.; Hanafy, Radwa A.; Couger, Matthew Brian; Stajich, Jason E.; Wang, Y.; Baker, Kristina; Dagar, Sumit Singh; Griffith, Gareth; Farag, Ibrahim; Callaghan, Tony M.

doi:10.1101/487215

Cited by 11 publications

(19 citation statements)

References 98 publications

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“…integration in eukaryotes 1,35 and this could be a strategy to diversify the original acquired function. 53…”

Section: Resultsmentioning

confidence: 99%

“…The publicly available genomes of 17 stramenopiles, 1 alveolate, 1 rhizarian and 1 haptophyte (listed 32 in Table S1) were downloaded and their nuclear proteomes, totalling to 398,001 protein-coding genes, 33 were searched for similarity in an all-against-all fashion with BLASTp (version 2.6+) using an e-value 34 cut-off of 10 -5 and retaining maximum 4,000 hits. Next, clustering of these protein-coding genes was 35 performed using OrthoFinder (version 2.1.2) 69 . 36…”

Section: Materials and Methods 30mentioning

confidence: 99%

“…While some studies used phylogenetics 7,30 , others relied purely on sequence 34 homology searches 24,25,27 . In this study, we sought to systematically detect HGT events simultaneously 35 across all sequenced diatoms. We delineated genes from horizontal descent using a high-throughput 36 gene family phylogenetics-based approach, which allows dating transfer events.…”

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confidence: 99%

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Systematic and functional analysis of horizontal gene transfer events in diatoms

Vancaester

Osuna-Cruz

Depuydt

et al. 2020

Preprint

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1.AbstractDiatoms are a diverse group of mainly photosynthetic algae, responsible for 20% of worldwide oxygen production, which can rapidly respond to favourable conditions and often outcompete other phytoplankton. We investigated the contribution of horizontal gene transfer (HGT) to its ecological success. A systematic phylogeny-based bacterial HGT detection procedure across nine sequenced diatoms showed that 3-5% of their proteome has a horizontal origin and a large influx occurred at the ancestor of diatoms. More than 90% of HGT genes are expressed, and species-specific HGT genes in Phaeodactylum tricornutum undergo strong purifying selection. They are implicated in several processes including environmental sensing, and expand the metabolic toolbox. Cobalamin (vitamin B12) is an essential cofactor for roughly half of the diatoms and is only produced by bacteria. Genes involved in its final synthesis were detected as HGT, including five consecutive enzymes in Fragilariopsis cylindrus. This might give diatoms originating from the Southern Ocean, a region typically depleted in cobalamin, a competitive advantage. Overall, we show that HGT is a prevalent mechanism that is actively used in diatoms to expand its adaptive capabilities.

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“…integration in eukaryotes 1,35 and this could be a strategy to diversify the original acquired function. 53…”

Section: Resultsmentioning

confidence: 99%

Section: Materials and Methods 30mentioning

confidence: 99%

mentioning

confidence: 99%

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Systematic and functional analysis of horizontal gene transfer events in diatoms

Vancaester

Osuna-Cruz

Depuydt

et al. 2020

Preprint

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“…Many of the corresponding protein-coding genes were also replicated within each fungal genome, demonstrating that individual rumen fungi hold several sets of functionally important genes. Despite a reportedly high degree of horizontal gene transfer (HGT) in the rumen microbiome 4,34,35 , only a few detected proteins mapped to both fungi and prokaryotes, suggesting that the overall sequences of these particular enzymes are evolutionary divergent across these two kingdoms.…”

Section: Taxonomic Origin Of Proteins Involved In Rumen Biomass-degramentioning

confidence: 99%

“…(sequence similarity ranging from 64 to 97% identity). Despite this seemingly conflicting result, this was not unexpected, given the scarcity of characterized fungal GH48s and the documented frequency of inter-kingdom horizontal gene transfer of catalytic domains in gut ecosystems 4,54 , especially for GH48s 55 . Nevertheless, while we postulate that these active GH48s originate from anaerobic fungi, likely achieved through HGT events, we cannot exclude that bacterial transcripts are present in the metatranscriptome.…”

Section: Supplementary Data S2) While Only Detected Amongst the Bactmentioning

confidence: 99%

Proteome specialization of anaerobic fungi during ruminal degradation of recalcitrant plant fiber

Hagen

Brooke

Shaw

et al. 2020

Preprint

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The rumen harbors a complex microbial mixture of archaea, bacteria, protozoa and fungi that efficiently breakdown plant biomass and its complex dietary carbohydrates into soluble sugars that can be fermented and subsequently converted into metabolites and nutrients utilized by the host animal. While rumen bacterial populations have been well documented, only a fraction of the rumen eukarya are taxonomically and functionally characterized, despite the recognition that they contribute to the cellulolytic phenotype of the rumen microbiota. To investigate how anaerobic fungi actively engage in digestion of recalcitrant fiber that is resistant to degradation, we resolved genome-centric metaproteome and metatranscriptome datasets generated from switchgrass samples incubated for 48 hours in nylon bags within the rumen of cannulated dairy cows. Across a gene catalogue covering anaerobic rumen bacteria, fungi and viruses, a significant portion of the detected proteins originated from fungal populations. Intriguingly, the carbohydrate-active enzyme (CAZyme) profile suggested a domain-specific functional specialization, with bacterial populations primarily engaged in the degradation of polysaccharides such as hemicellulose, whereas fungi were inferred to target recalcitrant cellulose structures via the detection of a number of endo-and exo-acting enzymes belonging to the glycoside hydrolase (GH) family 5, 6, 8 and 48. Notably, members of the GH48 family were amongst the highest abundant CAZymes and detected representatives from this family also included dockerin domains that are associated with fungal cellulosomes. A eukaryoteselected metatranscriptome further reinforced the contribution of uncultured fungi in the ruminal degradation of recalcitrant fibers. These findings elucidate the intricate networks of in situ recalcitrant fiber deconstruction, and importantly, suggests that the anaerobic rumen fungi contribute a specific set of CAZymes that complement the enzyme repertoire provided by the specialized plant cell wall degrading rumen bacteria.

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Enzymes of early-diverging, zoosporic fungi

Lange¹,

Barrett

Pilgaard

et al. 2019

Appl Microbiol Biotechnol

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The secretome, the complement of extracellular proteins, is a reflection of the interaction of an organism with its host or substrate, thus a determining factor for the organism’s fitness and competitiveness. Hence, the secretome impacts speciation and organismal evolution. The zoosporic Chytridiomycota , Blastocladiomycota , Neocallimastigomycota , and Cryptomycota represent the earliest diverging lineages of the Fungal Kingdom. The review describes the enzyme compositions of these zoosporic fungi, underscoring the enzymes involved in biomass degradation. The review connects the lifestyle and substrate affinities of the zoosporic fungi to the secretome composition by examining both classical phenotypic investigations and molecular/genomic-based studies. The carbohydrate-active enzyme profiles of 19 genome-sequenced species are summarized. Emphasis is given to recent advances in understanding the functional role of rumen fungi, the basis for the devastating chytridiomycosis, and the structure of fungal cellulosome. The approach taken by the review enables comparison of the secretome enzyme composition of anaerobic versus aerobic early-diverging fungi and comparison of enzyme portfolio of specialized parasites, pathogens, and saprotrophs. Early-diverging fungi digest most major types of biopolymers: cellulose, hemicellulose, pectin, chitin, and keratin. It is thus to be expected that early-diverging fungi in its entirety represents a rich and diverse pool of secreted, metabolic enzymes. The review presents the methods used for enzyme discovery, the diversity of enzymes found, the status and outlook for recombinant production, and the potential for applications. Comparative studies on the composition of secretome enzymes of early-diverging fungi would contribute to unraveling the basal lineages of fungi.

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Horizontal gene transfer as an indispensable driver for Neocallimastigomycota evolution into a distinct gut-dwelling fungal lineage

Cited by 11 publications

References 98 publications

Systematic and functional analysis of horizontal gene transfer events in diatoms

Systematic and functional analysis of horizontal gene transfer events in diatoms

Proteome specialization of anaerobic fungi during ruminal degradation of recalcitrant plant fiber

Enzymes of early-diverging, zoosporic fungi

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