Opportunities lost? Evolutionary causes and ecological consequences of the absence of trehalose digestion in birds

BRUN, ANTONIO; GUTIÉRREZ-GUERRERO; YOCELYN; MAGALLANES, MELISA E; CAVIEDES VIDAL, ENRIQUE; KARASOV, WILLIAM H.; MARTINEZ DEL RIO, CARLOS

PHYSIOLOGICAL AND BIOCHEMICAL ZOOLOGY

UNIV CHICAGO PRESS

Año: 2022 vol. 94 p. 340 - 349

1522-2152

Trehalose is a nonreducing disaccharide that is a primary storageand energy source in prokaryotes, yeasts, fungi, and invertebrates.Vertebrates digest trehalose with the intestinal brush bordermembrane (BBM) enzyme trehalase. Intestinal trehalase activityis reported to be either very low or absent in several bird species.We assayed trehalase activity in 19 avian species, used proteomicanalysis to quantify its abundance in the intestinal BBM, and usedanalyses of available genomes to detect the presence of the genethat codes for trehalase (Treh). We found no intestinal trehalaseactivity in birds, trehalase was absent from the proteome of theirintestinal BBM, and the gene coding for trehalase was absent intheir genomes. Surveys of available transcriptomes support thehypothesis thatTrehis absent in birds. The trehalase gene wasfound in the same conserved syntenic block within the genome ofall vertebrates surveyed except birds. Our analysis suggests thatTrehwas lost in an inversion followed by a reinsertion of a largegene block. This event appears to have taken place after the splitbetween crocodiles and birds and dinosaurs. Birds are unable todigest a common dietary sugar like trehalose because their an-cestor lost the trehalase gene. The loss of this gene seems to represent an ecological cost, as insectivorous birds seem to beunable to digest a carbohydrate present in their prey. We alsospeculate that the paucity of mycophagy in birds is due to thepresence of large amounts of this sugar in fungal tissues.