Multiple horizontally acquired genes from fungal and prokaryotic donors encode cellulolytic enzymes in the bdelloid rotifer Adineta ricciae

Szydłowski, Lesław; Boschetti, Chiara; Crisp, Alastair; Barbosa, Elton Gargioni Grisoste; Tunnacliffe, Alan

doi:10.1016/j.gene.2015.04.007

Cited by 24 publications

(18 citation statements)

References 93 publications

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“…Here we demonstrated that in each of the five Phytophaga beetles investigated, at least two of these GH45s possess cellulolytic activity. This discovery is in accordance with other previously described GH45 proteins from Insecta (Pauchet, Kirsch, et al 2014), Nematoda (Kikuchi, et al 2004), Mollusca (Rahman, et al 2014), Rotifera (Szydlowski, et al 2015) and microbes (Mcgavin and Forsberg 1988).…”

Section: Discussionsupporting

confidence: 93%

Functional analyses of the horizontally acquired Phytophaga glycoside hydrolase family 45 (GH45) proteins reveal distinct functional characteristics

Busch

Pauchet

2018

Preprint

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14Cellulose, a major polysaccharide of the plant cell wall, consists of β-1,4-linked glucose moieties 15 forming a molecular network recalcitrant to enzymatic breakdown. Although cellulose is 16 potentially a rich source of energy, the ability to degrade it is rare in animals and was believed to 17 be present only in cellulolytic microbes. Recently, it has become clear that some animals encode 18 endogenous cellulases belonging to several glycoside hydrolase families (GHs), including GH45. 19GH45s are distributed patchily among the Metazoa and, in insects, are encoded only by the 20 genomes of Phytophaga beetles. This study aims to understand both the enzymatic properties and 21 the evolutionary history of GH45s in these beetles. To this end, we tested the enzymatic abilities 22 of 37 GH45s derived from five species of Phytophaga beetles and learned that beetle-derived 23 GH45s degrade three different substrates: amorphous cellulose, xyloglucan and glucomannan. 24Our phylogenetic and gene structure analyses indicate that at least one gene encoding a putative 25 cellulolytic GH45 was present in the last common ancestor of the Phytophaga, and that GH45 26 xyloglucanases evolved several times independently in these beetles. The most closely related 27 clade to Phytophaga GH45s contained fungal sequences, suggesting this GH family was acquired 28 by horizontal gene transfer from fungi. Other than in insects, arthropod GH45s do not share a 29 common origin and appear to have emerged at least three times independently. 30 31

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Section: Discussionsupporting

confidence: 93%

Functional analyses of the horizontally acquired Phytophaga glycoside hydrolase family 45 (GH45) proteins reveal distinct functional characteristics

Busch

Pauchet

2018

Preprint

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“…Functional horizontal gene transfer (fHGT) can bring to a recipient genome new biochemical capacities and contrasts with gradualist evolution of endogenous genes to new function. The bdelloid rotifers Adineta vaga (28) and Adineta ricciae (29) have high levels of fHGT (∼8%), and this has been associated with both their survival as phylogenetically ancient asexuals and their ability to undergo cryptobiosis (28)(29)(30)(31)(32). Different kinds of evidence are required to support claims of doaHGT compared with fHGT.…”

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confidence: 99%

No evidence for extensive horizontal gene transfer in the genome of the tardigrade Hypsibius dujardini

Koutsovoulos

Kumar

Laetsch

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

232

198

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Tardigrades are meiofaunal ecdysozoans that are key to understanding the origins of Arthropoda. Many species of Tardigrada can survive extreme conditions through cryptobiosis. In a recent paper [Boothby TC, et al. (2015) Proc Natl Acad Sci USA 112(52):15976-15981], the authors concluded that the tardigrade Hypsibius dujardini had an unprecedented proportion (17%) of genes originating through functional horizontal gene transfer (fHGT) and speculated that fHGT was likely formative in the evolution of cryptobiosis. We independently sequenced the genome of H. dujardini. As expected from whole-organism DNA sampling, our raw data contained reads from nontarget genomes. Filtering using metagenomics approaches generated a draft H. dujardini genome assembly of 135 Mb with superior assembly metrics to the previously published assembly. Additional microbial contamination likely remains. We found no support for extensive fHGT. Among 23,021 gene predictions we identified 0.2% strong candidates for fHGT from bacteria and 0.2% strong candidates for fHGT from nonmetazoan eukaryotes. Cross-comparison of assemblies showed that the overwhelming majority of HGT candidates in the Boothby et al. genome derived from contaminants. We conclude that fHGT into H. dujardini accounts for at most 1-2% of genes and that the proposal that onesixth of tardigrade genes originate from functional HGT events is an artifact of undetected contamination.tardigrade | blobtools | contamination | metagenomics | horizontal gene transfer

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“…The functional diversity of the GH16 proteins has been well studied in insects, including the identification of a highly modified version of these enzymes as a GNBP and of a unique conserved b-1,3-glucan binding domain that is important for innate immune recognition in insects (Hughes, 2012). It was reported that during the course of evolution, the GH16 proteins have evolved to possess b-1,3-glucanase activity with a nonfunctional GNBP domain (Hughes, 2012;Szydlowski et al, 2015). The phylogenetic analysis of GH16 forms two clusters, which represent the group of active b-1,3-glucanases and the diversified b-1-3-glucan binding domain proteins.…”

Section: Discussionmentioning

confidence: 99%

Identification and expression profiling of novel plant cell wall degrading enzymes from a destructive pest of palm trees, Rhynchophorus ferrugineus

Antony

Johny

Aldosari

et al. 2017

Insect Molecular Biology

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Plant cell wall degrading enzymes (PCWDEs) from insects were recently identified as a multigene family of proteins that consist primarily of glycoside hydrolases (GHs) and carbohydrate esterases (CEs) and play essential roles in the degradation of the cellulose/hemicellulose/pectin network in the invaded host plant. Here we applied transcriptomic and degenerate PCR approaches to identify the PCWDEs from a destructive pest of palm trees, Rhynchophorus ferrugineus, followed by a gut-specific and stage-specific differential expression analysis. We identified a total of 27 transcripts encoding GH family members and three transcripts of the CE family with cellulase, hemicellulase and pectinase activities. We also identified two GH9 candidates, which have not previously been reported from Curculionidae. The gut-specific quantitative expression analysis identified key cellulases, hemicellulases and pectinases from R. ferrugineus. The expression analysis revealed a pectin methylesterase, RferCE8u02, and a cellulase, GH45c34485, which showed the highest gut enriched expression. Comparison of PCWDE expression patterns revealed that cellulases and pectinases are significantly upregulated in the adult stages, and we observed specific high expression of the hemicellulase RferGH16c4170. Overall, our study revealed the potential of PCWDEs from R. ferrugineus, which may be useful in biotechnological applications and may represent new tools in R. ferrugineus pest management strategies.

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Multiple horizontally acquired genes from fungal and prokaryotic donors encode cellulolytic enzymes in the bdelloid rotifer Adineta ricciae

Cited by 24 publications

References 93 publications

Functional analyses of the horizontally acquired Phytophaga glycoside hydrolase family 45 (GH45) proteins reveal distinct functional characteristics

Functional analyses of the horizontally acquired Phytophaga glycoside hydrolase family 45 (GH45) proteins reveal distinct functional characteristics

No evidence for extensive horizontal gene transfer in the genome of the tardigrade Hypsibius dujardini

Identification and expression profiling of novel plant cell wall degrading enzymes from a destructive pest of palm trees, Rhynchophorus ferrugineus

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