The symbiotic lignocellulose degradation in termite guts: Novel insights into main bacterial players and mechanisms, with focus on the phylum Fibrobacterota
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Philipps-Universität Marburg
Abstract
The microbial landscape within termite guts varies across termite families. The gut
microbiota of lower termites (LT) is dominated by cellulolytic flagellates that sequester
wood particles in their digestive vacuoles, whereas in the flagellate-free higher termites
(HT), cellulolytic activity has been attributed to fiber-associated bacteria. However, little
is known about the role of individual lineages of bacteria in fiber digestion, particularly
in LT.
In this study, I investigated the lignocellulolytic potential of 2,223 metagenome-
assembled genomes (MAGs) recovered from the gut metagenomes of 51 termite
species. In the flagellate-dependent LT, cellulolytic enzymes are restricted to MAGs of
Bacteroidota (Dysgonomonadaceae, Tannerellaceae, Bacteroidaceae,
Azobacteroidaceae) and Spirochaetota (Breznakiellaceae) and reflect a specialization
on cellodextrins, whereas their hemicellulolytic arsenal features activities on xylans
and diverse heteropolymers. By contrast, in MAGs derived from flagellate-free HT, I
detected cellulose-oxidizing and lignin-modifying enzymes assigned to the phyla
Pseudomonadota (Burkholderiales, Pseudomonadales) and Actinomycetota
(Actinomycetales, Mycobacteriales) located at the hindgut wall. Furthermore, in these
termites, Spirochaetota and Fibrobacterota possess a comprehensive arsenal of exo-
and endoglucanases that resembles that of LT gut flagellates, underlining they occupy
this cellulolytic niche in higher termites.
Previous studies into the Fibrobacterota have focused on the type species, Fibrobacter
succinogenes, as well as the only genome representative from termites, Candidatus
Fibromonas termitidis, and have shown these bacteria actively colonize the wood
particles, creating biofilms to degrade the cellulose. I therefore investigated 111
Fibrobacterota MAGs, along with metatranscriptomes from the hindgut of wood-
feeding HT, extending the knowledge of gene expression to termite groups from all
families within the phylum. Our results confirm that the phylum employs a multi-protein
complex involving type IX-like secretion systems, type IV pili and tonB-dependant
importers to colonize the wood, coordinate the delivery of cellulases, as well as to
uptake products, such as cellodextrin and metabolites. This is powered by a unique
metabolism that drives a strong proton-motive force to keep fueling cellulolysis and
fermentation. In the termite-symbiotic Ca. Fibromonas, similar fermentation products
as the mammal-symbiotic Fibrobacter are predicted, with exception of formate. We
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confirm, furthermore, this termite lineage is capable of oxygen respiration, a seemingly
unique capacity within the phylum. Termite-symbiotic Chitinivibrionia, the other class
within the phylum, are predicted to produce hydrogen gas, acetate and ethanol, but
not formate, unlike the extreme alkaliphilic lineages represented by the sister type
species Chitivibrio alkaliphilus and Chitinispirillum alkaliphilum. We discuss the
different metabolic and electron transport pathways in the lineages also in light of the
capacity of biosynthesis of the cofactors heme and cobalamin.
The results of this study refine our concept of symbiotic digestion of lignocellulose in
termite guts, emphasizing the differential roles of specific bacterial lineages in both
flagellate-dependent and flagellate-independent breakdown of cellulose and
hemicelluloses. Furthermore, this study sheds light on the previously cryptic cellulolytic
mechanism employed by the Fibrobacterota in the gut of wood-feeding higher termites,
proposing a biofilm-associated process. Lastly, it also unveils a so far unappreciated
role of oxygen in the depolymerization of plant fiber and lignin in the microoxic
periphery during gut passage in HT.
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