Soil organic matter is essential for colony growth in subterranean termites

Aaron Mullins,Thomas Chouvenc,Nan-Yao Su

doi:10.1038/s41598-021-00674-z

Aaron Mullins, Thomas Chouvenc + Show 1 more

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https://doi.org/10.1038/s41598-021-00674-z

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Abstract

Intrinsic dinitrogen (N2) fixation by diazotrophic bacteria in termite hindguts has been considered an important pathway for nitrogen acquisition in termites. However, studies that supported this claim focused on measuring instant N2 fixation rates and failed to address their relationship with termite colony growth and reproduction over time. We here argue that not all wood-feeding termites rely on symbiotic diazotrophic bacteria for colony growth. The present study looks at dietary nitrogen acquisition in a subterranean termite (Rhinotermitidae, Coptotermes). Young termite colonies reared with wood and nitrogen-rich organic soil developed faster, compared to those reared on wood and inorganic sand. More critically, further colony development was arrested if access to organic soil was removed. In addition, no difference of relative nitrogenase expression rates was found when comparing the hindguts of termites reared between the two conditions. We therefore propose that subterranean termite (Rhinotermitidae) colony growth is no longer restricted to metabolically expensive intrinsic N2 fixation, as the relationship between diazotrophic bacteria and subterranean termites may primarily be trophic rather than symbiotic. Such reliance of Rhinotermitidae on soil microbial decomposition activity for optimal colony growth may also have had a critical mechanistic role in the initial emergence of Termitidae.

Highlights

It has been proposed that a problem fundamental to most insect/diazotroph investigations is that they primarily focus on only one of three aspects of the phenomenon[30]
In wood-feeding termites, carbon is not a limiting factor for such growth; our study demonstrated that a lack of access to dietary nitrogen is a fundamental limiting factor for initial colony growth in C. formosanus
We suspected that lack of access to soil micronutrients may be a limiting factor to intrinsic nitrogenase activity of termite diazotrophic gut bacterial mutualists, and any increase in nitrogen following colony growth could be the result of increased nitrogen fixation in worker hindguts, rather than of dietary origin

Summary

Introduction

It has been proposed that a problem fundamental to most insect/diazotroph investigations is that they primarily focus on only one of three aspects of the phenomenon[30]. It was suggested that some termite species may acquire nitrogen both through symbiotic N 2 fixation and selective foraging within their behavioral r epertoire[46] Such combined observations lend credence to our hypothesis that while some termite species may be able to fix atmospheric N2 in their hindgut as means of primary nitrogen procurement, other termites may forego this metabolically expensive process when alternative, dietary sources of nitrogen are available for significant colony growth. A study comparing metagenomic profiles between termites exhibiting one-piece and extended life types suggested that dietary nitrogen may be utilized as a supplement to an all-wood d iet[47] These observations beg the question of whether nitrogen-rich soil OM is a primary source of nitrogen for a growing colony of C. formosanus.

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