The fungal symbiont of Acromyrmex leaf-cutting ants expresses the full spectrum of genes to degrade cellulose and other plant cell wall polysaccharidesReportar como inadecuado




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BMC Genomics

, 14:928

Eukaryote microbial genomics

Abstract

BackgroundThe fungus gardens of leaf-cutting ants are natural biomass conversion systems that turn fresh plant forage into fungal biomass to feed the farming ants. However, the decomposition potential of the symbiont Leucocoprinus gongylophorus for processing polysaccharides has remained controversial. We therefore used quantifiable DeepSAGE technology to obtain mRNA expression patterns of genes coding for secreted enzymes from top, middle, and bottom sections of a laboratory fungus-garden of Acromyrmex echinatior leaf-cutting ants.

ResultsA broad spectrum of biomass-conversion-relevant enzyme genes was found to be expressed in situ: cellulases GH3, GH5, GH6, GH7, AA9 formerly GH61, hemicellulases GH5, GH10, CE1, GH12, GH74, pectinolytic enzymes CE8, GH28, GH43, PL1, PL3, PL4, glucoamylase GH15, α-galactosidase GH27, and various cutinases, esterases, and lipases. In general, expression of these genes reached maximal values in the bottom section of the garden, particularly for an AA9 lytic polysaccharide monooxygenase and for a GH5 endocellulase, a GH7 reducing end-acting cellobiohydrolase, and a GH10 xylanase, all containing a carbohydrate binding module that specifically binds cellulose CBM1. Although we did not directly quantify enzyme abundance, the profile of expressed cellulase genes indicates that both hydrolytic and oxidative degradation is taking place.

ConclusionsThe fungal symbiont of Acromyrmex leaf-cutting ants can degrade a large range of plant polymers, but the conversion of cellulose, hemicellulose, and part of the pectin occurs primarily towards the end of the decomposition process, i.e. in the bottom section of the fungus garden. These conversions are likely to provide nutrients for the fungus itself rather than for the ants, whose colony growth and reproductive success are limited by proteins obtained from ingesting fungal gongylidia. These specialized hyphal tips are hardly produced in the bottom section of fungus gardens, consistent with the ants discarding old fungal biomass from this part of the garden. The transcripts that we found suggest that actively growing mycelium in the bottom of gardens helps to maintain an optimal water balance to avoid hyphal disintegration, so the ants can ultimately discard healthy rather than decaying and diseased garden material, and to buffer negative effects of varying availability and quality of substrate across the seasons.

KeywordsAcromyrmex echinatior Attine ants Biomass conversion Carbohydrate-active enzymes CAZymes DeepSAGE Fungus garden Leucocoprinus gongylophorus Symbiosis Transcript profiling AbbreviationsAAAuxiliary activity

ANOVAAnalysis of variance

CBHCellobiohydrolase

CBMCarbohydrate-binding module

CECarbohydrate esterase

DeepSAGEDeep serial analysis of gene expression

ESTExpressed sequence tag

GHGlycoside hydrolase

PDAPotato dextrose agar

PLPolysaccharide lyase

PPRPeptide pattern recognition

WBAWheat bran agar.

Electronic supplementary materialThe online version of this article doi:10.1186-1471-2164-14-928 contains supplementary material, which is available to authorized users.

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Autor: Morten N Grell - Tore Linde - Sanne Nygaard - Kåre L Nielsen - Jacobus J Boomsma - Lene Lange

Fuente: https://link.springer.com/



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