Dietary‐driven variation effects on the symbiotic flagellate protist communities of the subterranean termite Reticulitermes grassei Clément

Abstract

The ability of subterranean termites to digest lignocellulose relies not only on their digestive tract physiology, but also on the symbiotic relationships established with flagellate protists and bacteria. The objective of this work was to test the possible effect of different cellulose‐based diets on the community structure (species richness and other diversity metrics) of the flagellate protists of the subterranean termite Reticulitermes grassei. Termites belonging to the same colony were subjected to six different diets (natural diet, maritime pine wood, European beech, thermally modified European beech, cellulose powder and starvation), and their flagellate protist community was evaluated after the trials. All non‐treated sound woods produced similar flagellate protist communities that were more diverse and of high evenness (low dominance). On the contrary, flagellate protist communities from cellulose‐fed termites and starving termites were considered to be significantly different from all non‐treated woods; they were less diverse and some morphotypes became dominant as a consequence of flagellate protist communities having suffered major adaptations to these diets. The flagellate protist communities of untreated beech and thermally modified beech‐fed termites were considered to be significantly different in terms of abundance and morphotype diversity. This may be caused by a decrease in lignocellulose quality available for termites and from an interference of thermally treated wood with the chemical stability of the termite hindgut. Our study suggests that as a consequence of the strong division of labour among these protists to accomplish the intricate process of lignocellulose digestion, termite symbiotic flagellate protist communities are a dynamic assemblage able to adapt to different conditions and diets. This study is important for the community‐level alteration approach, and it is the first study to investigate the effects of thermally modified wood on the flagellate protist communities of subterranean termites.

Efficient but occasionally imperfect vertical transmission of gut mutualistic protists in a wood‐feeding termite

“…More specifically, this study provides the first metabarcoding data on Preaxostyla protists of the order Oxymonadida. Our results revealed a high diversity of oxymonad OTUs, all of which were assigned to the two genera so far described in Reticulitermes species, namely Pyrsonympha and Dinenympha (Duarte, Duarte, Borges, & Nunes, ; Kitade & Matsumoto, ; Lewis & Forschler, ; Shimada, Lo, Kitade, Wakui, & Maekawa, ; Stingl & Brune, ; Yamin, ). For parabasalid protists, the richness of OTUs was comparable to that of a previous metabarcoding studies on R. grassei (Waidele et al, ).…”

The gut bacteria across life stages in the synanthropic fly Chrysomya megacephala

“…Insect gut bacteria are closely associated with feed digestion [ 7 ], especially for specific food types, such as blood-sucking bugs and wood/soil-consuming termites and herbivorous insects [ 8 – 11 ]. Gut bacteria mining of herbivorous insects with typical cultural method and metagenome sequencing was conducted to identify beneficial microbes that possess cellulase activity [ 12 , 13 ]. Parallel saprophagous fly Musca domestica larval gut was reported as a digestion chamber altered antibiotic resistome of swine manure other than merely digested manure [ 14 ].…”

Symbiotic flagellate protists as cryptic drivers of adaptation and invasiveness of the subterranean termite Reticulitermes grassei Clément

“…A geographical pattern is suggested in the dissimilarity analysis, which allowed to discriminate some geographical groups, although, for example, the three most diverse flagellate protist communities are grouped together regardless of their geographical origin (hor1, hor2, and ses; see Figure ); however, the local factors seem to have a major role on the determination of the flagellate protist community variability and/or eventually natural variation should also be considered. The termite diet is one of such influential local factors on the flagellate protist communities of R. grassei belonging to the same colony (Duarte, Duarte et al., ). However, regarding termites in their natural range, it is very difficult to identify or specify the actual food ingested whatever the type of sources addressed during the observation of foraging; such ingested materials probably comprise a subset of the available cellulolytic material.…”

“…Generally, the termite flagellate protist species are under strong co‐evolutionary constraints, and the major part of gut symbionts is endemic or native and probably co‐evolving with termite species (Hongoh et al., ; Noda et al., ). Evolutionary constraints may be closely linked with the specificity of the role of each flagellate protist in the different phases of the lignocellulose digestion process, which also dictates an environmental or functional filtering (meaning that only one species, or group of species, is able to occupy a certain ecological niche), as there exists a division of labor during the lignocellulose digestion process (Duarte, Duarte et al., ; Inoue, Murashima, Azuma, Sugimoto, & Slaytor, ; Raychoudhury et al., ; Todaka et al., ; Yoshimura, Fujino, Tsunoda, & Takahashi, ). Furthermore, the existence of a core group seems to be crucial for the maintenance of the termite holobiont, while other species may vary in function of the environment.…”

“…Twenty worker termites in the 4th instar of development per sampling point were analyzed individually in terms of symbiont protists diversity and abundance by direct observation under a microscope. For quantification of flagellate protists, a hemocytometer was used, in accordance with a previously described method (Duarte, Duarte, Borges, & Nunes, ), with an adaptation in the calculations for the number of flagellate protists per microliter of hindgut fluid, which were estimated to the observed area of the hemocytometer following the formula: N is the number of cells visualized, S q is the number of squares, and D f is the dilution factor.…”