Transformation and Mineralization of Organic Matter by the Humivorous Larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae)

Abstract

Scarabaeidae beetle larvae are widely distributed in various ecosystems, which numerous species that either co-operate in soil processes or at least live in soil at some stage in their development, and play important roles in organic matter transformation and soil development. The larvae of Scarabaeidae have been mainly considered in the context of fiber degradation, e.g., the digestion of plant biomass in various stages of decomposition. However, their food spectrum is apparently much broader than generally assumed. In this study, the transformation and mineralization of organic matter during gut passage were investigated using the larva of the cetoniid beetle Pachnoda ephippiata (Coleoptera: Scarabaeidae) as a humus-feeding model organism with a highly alkaline gut.In order to investigate whether microbial biomass and its residues and humic substances are nutrient and energy sources for humivorous beetle larvae, we carried out feeding trials using soil supplemented with 14C-labeled fungal biomass (Penicillium chrysogenum), bacterial biomass (Bacillus megaterium), fungal or bacterial structural polysaccharides (chitin, peptidoglycan), bacterial protein, or cellulose, and specifically 14C-labeled model humic acids synthesized by peroxidase-initiated radical polymerization.The results showed that gut passage strongly stimulated the mineralization of the structural polymers. The amount of radiolabel recovered from the body and hemolymph of the larvae indicated that microbial biomass and its structural components were assimilated more efficiently than cellulose. Larvae significantly increased the mineralization of humic acids labeled in their peptide or polysaccharide components, whereas the mineralization of humic acids labeled in the aromatic components did not increase significantly. The degradation of these materials mainly occurred in the alkaline midgut. The potential degradation rate of peptides to TCA-soluble products in the midgut homogenate was about 24-fold higher than that of humic-acid-stabilized peptide. Degradation rates of peptidoglycan and chitin were lower than that of peptide. Midgut contains high concentrations of soluble protein and amino acids. Incubation of midgut homogenates with soil released amino acids at a considerable rate, which explains the high in vivo concentrations of amino acids observed in the midgut.Microbial dissimilatory iron reduction occurred during gut passage. One of dominant (hemi)cellulose-degrading bacterial species isolated from the hindgut of the larva, Promicromonospora pachnodae, was capable of reducing iron, providing a strong indication that dissimilatory iron reduction may involve in the processes of organic matter degradation in the intestinal tract.This study presents the first direct evidence that microbial biomass and nitrogenous and polysaccharide components of humic acids are preferentially degraded in the intestinal tract and constitute potential food sources for humivorous beetle larvae. In contrast, aromatic components of humic acid were not an important food source. The combined evidence proved that alkaline extraction of recalcitrant organic matter, host enzymes, and microbial fermentations during gut passage are keys for the transformation and mineralization of organic matter.During gut passage, ingested organic matter underwent selective digestion and humification, which enhanced the stability of the organic residues in the feces. Gut passage would significantly alter the nitrogen cycling rate, and the forms and the distribution of nitrogen in the soil.