Abstract

Previous surveys of the gut microbiota of termites have been limited to the worker caste. Termite gut microbiota has been well documented over the last decades and consists mainly of lineages specific to the gut microbiome which are maintained across generations. Despite this intimate relationship, little is known of how symbionts are transmitted to each generation of the host, especially in higher termites where proctodeal feeding has never been reported. The bacterial succession across life stages of the wood-feeding higher termite Nasutitermes arborum was characterized by 16S rRNA gene deep sequencing. The microbial community in the eggs, mainly affiliated to Proteobacteria and Actinobacteria, was markedly different from the communities in the following developmental stages. In the first instar and last instar larvae and worker caste termites, Proteobacteria and Actinobacteria were less abundant than Firmicutes, Bacteroidetes, Spirochaetes, Fibrobacteres and the candidate phylum TG3 from the last instar larvae. Most of the representatives of these phyla (except Firmicutes) were identified as termite-gut specific lineages, although their relative abundances differed. The most salient difference between last instar larvae and worker caste termites was the very high proportion of Spirochaetes, most of which were affiliated to the Treponema Ic, Ia and If subclusters, in workers. The results suggest that termite symbionts are not transmitted from mother to offspring but become established by a gradual process allowing the offspring to have access to the bulk of the microbiota prior to the emergence of workers, and, therefore, presumably through social exchanges with nursing workers.

Highlights

  • Gut microbial symbionts enable termites to play a key role in ecosystem processes such as carbon and nitrogen cycling

  • As only 50 non-Wolbachia reads remained from L1 larvae, this development stage was not included for downstream analysis

  • Most of the operational taxonomic units (OTU) fell within the following phyla: Proteobacteria (31.46%), Spirochaetes (27.94%), Bacteroidetes (15.44%), Firmicutes (7.27%), Actinobacteria (6.02%), Fibrobacteres (4.71%), Candidate phylum TG3 (4.54%), Acidobacteria (0.98%) and Synergistetes (0.29%)

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Summary

Introduction

Gut microbial symbionts enable termites to play a key role in ecosystem processes such as carbon and nitrogen cycling. Specific termite gut microbiota was found in the congeneric soilfeeding species C. ortognathus from a Kenyan grassland and C. niokolensis from a Senegalese savannah [2]. The presence of gut-specific Actinobacteria has been reported in the wood-feeding termite species, Nasutitermes corniger Motschulsky, collected from various geographical sites [3]. The gut of wood-feeding species that feed on lignocellulose components is mainly colonized by Spirochaetes and members of the Fibrobacteres phylum and related candidate phylum TG3 while the gut community of soil-feeders which thrive on nitrogen-rich components is dominated by Firmicutes. In fungus-growing species, the dominant phyla are Bacteroidetes and Firmicutes. Both host phylogeny and diet can be important determinants of the bacterial community structure in termite guts [5,6,7]

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