Nest composition, stable isotope ratios and microbiota unravel the feeding behaviour of an inquiline termite

Hellemans, Simon; Marynowska, Martyna; Drouet, Thomas; Lepoint, Gilles; Fournier, Denis; Całusińska, Magdalena; Roisin, Yves

doi:10.1007/s00442-019-04514-w

Cited by 6 publications

(7 citation statements)

References 77 publications

(105 reference statements)

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“…Microbial communities of termite mounds are entirely distinct from those of termite guts (42)(43)(44)(45)(46). Whereas primarily anaerobic fermentative Firmicutes, Bacteroidota, and Spirochaetota dominate in guts, potentially aerobic respiratory Actinobacteriota, Proteobacteria, and Acidobacteriota reside in mounds.…”

Section: Significancementioning

confidence: 99%

Termite gas emissions select for hydrogenotrophic microbial communities in termite mounds

Chiri

Nauer

Lappan

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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Organoheterotrophs are the dominant bacteria in most soils worldwide. While many of these bacteria can subsist on atmospheric hydrogen (H2), levels of this gas are generally insufficient to sustain hydrogenotrophic growth. In contrast, bacteria residing within soil-derived termite mounds are exposed to high fluxes of H2 due to fermentative production within termite guts. Here, we show through community, metagenomic, and biogeochemical profiling that termite emissions select for a community dominated by diverse hydrogenotrophic Actinobacteriota and Dormibacterota. Based on metagenomic short reads and derived genomes, uptake hydrogenase and chemosynthetic RuBisCO genes were significantly enriched in mounds compared to surrounding soils. In situ and ex situ measurements confirmed that high- and low-affinity H2-oxidizing bacteria were highly active in the mounds, such that they efficiently consumed all termite-derived H2 emissions and served as net sinks of atmospheric H2. Concordant findings were observed across the mounds of three different Australian termite species, with termite activity strongly predicting H2 oxidation rates (R2 = 0.82). Cell-specific power calculations confirmed the potential for hydrogenotrophic growth in the mounds with most termite activity. In contrast, while methane is produced at similar rates to H2 by termites, mounds contained few methanotrophs and were net sources of methane. Altogether, these findings provide further evidence of a highly responsive terrestrial sink for H2 but not methane and suggest H2 availability shapes composition and activity of microbial communities. They also reveal a unique arthropod–bacteria interaction dependent on H2 transfer between host-associated and free-living microbial communities.

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Section: Significancementioning

confidence: 99%

Termite gas emissions select for hydrogenotrophic microbial communities in termite mounds

Chiri

Nauer

Lappan

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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“…The pre-digested lignocellulose may especially attract commensal species, inquilines or kleptoparasitic termites (mound-/soil- or humus-feeding species) such as Macrognathotermes sunteri found on Coptotermes acinaciformis mounds or Cavitermes tuberosus , on Labiotermes labralis , Termes fatalis or Neocapritermes taracua mounds, or Inquilinitermes microcerus found in Constrictotermes cyphergaster mounds (note a wide variety of termite species may inhabit opportunistically the mounds built by other termite species) [3] , [117] , [118] , [119] , [120] , [121] . Some inquiline species feed on the already digested (pseudo-) faeces within the mound matrix of their host, e.g.…”

Section: Termite Structures As Functional Materialsmentioning

confidence: 99%

“…tuberosus Termitidae, (iii) S. America arboreal/ soil inquiline to (18)(20) irregular; concave trunk sect. ; [119] , [214] (18) La. labralis Syntermitinae, (iii) S. America mound/soil 110 liters =

m 3 alveolar, carton & at tree base; [65] (19) La.…”

Section: Overview Tablementioning

confidence: 99%

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Revisiting stigmergy in light of multi-functional, biogenic, termite structures as communication channel

Oberst

Lai

Martin

et al. 2020

Computational and Structural Biotechnology Journal

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Termite mounds are fascinating because of their intriguing composition of numerous geometric shapes and materials. However, little is known about these structures, or of their functionalities. Most research has been on the basic composition of mounds compared with surrounding soils. There has been some targeted research on the thermoregulation and ventilation of the mounds of a few species of fungi-growing termites, which has generated considerable interest from human architecture. Otherwise, research on termite mounds has been scattered, with little work on their explicit properties. This review is focused on how termites design and build functional structures as nest, nursery and food storage; for thermoregulation and climatisation; as defence, shelter and refuge; as a foraging tool or building material; and for colony communication, either as in indirect communication (stigmergy) or as an information channel essential for direct communication through vibrations (biotremology). Our analysis shows that systematic research is required to study the properties of these structures such as porosity and material composition. High resolution computer tomography in combination with nonlinear dynamics and methods from computational intelligence may provide breakthroughs in unveiling the secrets of termite behaviour and their mounds. In particular, the examination of dynamic and wave propagation properties of termite-built structures in combination with a detailed signal analysis of termite activities is required to better understand the interplay between termites and their nest as superorganism. How termite structures serve as defence in the form of disguising acoustic and vibration signals from detection by predators, and what role local and global vibration synchronisation plays for building are open questions that need to be addressed to provide insights into how termites utilise materials to thrive in a world of predators and competitors.

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“…The gallery-associated bacterial OTUs identified in this study mostly belonged to Proteobacteria and Actinobacteria, which are known to dominate the nest bacterial communities of several Termitidae species (Hellemans et al 2019). A total of 18 OTUs belonged to Proteobacteria, including seven OTUs assigned to Rhizobiales, five of which were identified as gallery-associated bacteria for the three termite species investigated in this study.…”

Section: Discussionmentioning

confidence: 71%

Termites are associated with external species-specific bacterial communities

et al.

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All termites have established a wide range of associations with symbiotic microbes in their guts. Some termite species are also associated with microbes that grow in their nests, but the prevalence of these associations remains largely unknown. Here, we studied the bacterial communities associated with the termites and galleries of three wood-feeding termite species using 16S rRNA amplicon sequencing. We found that the composition of bacterial communities differs among termite bodies, termite galleries, and control wood fragments devoid of termite activities, in a species-specific manner. Termite galleries were enriched in bacterial OTUs belonging to Rhizobiales and Actinobacteria, which were often shared by several termite species. The abundance of several bacterial OTUs, generally belonging to genera known to include animal pathogens, was depleted in termite galleries. Our results demonstrate that termites not only harbour unique bacterial communities inside their guts, but also shape the communities colonizing their nests and galleries.

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Nest composition, stable isotope ratios and microbiota unravel the feeding behaviour of an inquiline termite

Cited by 6 publications

References 77 publications

Termite gas emissions select for hydrogenotrophic microbial communities in termite mounds

Termite gas emissions select for hydrogenotrophic microbial communities in termite mounds

Revisiting stigmergy in light of multi-functional, biogenic, termite structures as communication channel

Termites are associated with external species-specific bacterial communities

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