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Profiling the Succession of Bacterial Communities throughout the Life Stages of a Higher Termite Nasutitermes arborum (Termitidae, Nasutitermitinae) Using 16S rRNA Gene Pyrosequencing.

Diouf M, Roy V, Mora P, Frechault S, Lefebvre T, Hervé V, Rouland-Lefèvre C, Miambi E - PLoS ONE (2015)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Département SOLéO, Institut d'Ecologie et des Sciences de l'Environnement de Paris (IEES), Université Paris Est Créteil (U-PEC), Bâtiment P4, 61 avenue du Général de Gaulle, 94010, Créteil, France.

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.

No MeSH data available.


Related in: MedlinePlus

Venn diagram of bacterial OTUs (at 97% identity) common to the pyrosequencing libraries for eggs (E), L2 larvae (L2) and workers (W) of N. arborum.Numbers in bold indicate the number of OTUs and numbers in italics the relative abundance of the corresponding OTUs in each stage where they are detected. Details of the common OTUs are given in S2 Table.
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pone.0140014.g003: Venn diagram of bacterial OTUs (at 97% identity) common to the pyrosequencing libraries for eggs (E), L2 larvae (L2) and workers (W) of N. arborum.Numbers in bold indicate the number of OTUs and numbers in italics the relative abundance of the corresponding OTUs in each stage where they are detected. Details of the common OTUs are given in S2 Table.

Mentions: Only two OTUs, accounting for less than 1% in all the pyrotag libraries, were common to the eggs, L2 larvae and worker caste termites of Nasutitermes arborum (Fig 3). These were Bacteroidetes affiliated to the M2PB4-61 Termite group (Rikenellaceae) and the higher termite a cluster (Rs-E47 termite group) respectively (S2 Table). Three OTUs were found in the eggs and L2 larvae and not in workers. They were from the genera Staphylococcus (Staphylococcaceae, Firmicutes), Massilia–6 (Oxalobacteraceae, Betaproteobacteria) and Subcluster Vb (Cluster Vb, Bacteroidetes) and together accounted for about 0.5% of reads in each of these stages. Sixteen OTUs were found in the eggs and worker caste termites but were not found in L2 Larvae. These common OTUs accounted for 6.3% and 18.9% of reads in eggs and workers respectively. They were primarily Firmicutes (5 OTUs, 1.76% or reads from eggs), Actinobacteria (4 OTUs, 2.71%) and Proteobacteria (4 OTUs, 1.39%). 16 OTUs were found in both L2 larvae and workers but not in other stages. There was a higher proportion of these common OTUs in L2 larvae (31.4% of reads), mainly from Bacteroidetes (10 OTUs, 24.36% of reads) especially from the M2PB4-65 termite group, from Treponema Ic cluster of Spirochetes (2 OTUs, 5.78% of reads in L2 larvae) and from Firmicutes (3 OTUs, 0.58% of reads in L2 larvae). These results indicate that there are significantly fewer OTUs in common between developmental stages than OTUs found only in one stage, which represented up to 92.4% of reads (or 70.53% of OTUs) from eggs, 68.4% reads (or 92.92% of OTUs) from L2 larvae, and 74.8% of reads (90.47% of OTUs) from the worker caste.


Profiling the Succession of Bacterial Communities throughout the Life Stages of a Higher Termite Nasutitermes arborum (Termitidae, Nasutitermitinae) Using 16S rRNA Gene Pyrosequencing.

Diouf M, Roy V, Mora P, Frechault S, Lefebvre T, Hervé V, Rouland-Lefèvre C, Miambi E - PLoS ONE (2015)

Venn diagram of bacterial OTUs (at 97% identity) common to the pyrosequencing libraries for eggs (E), L2 larvae (L2) and workers (W) of N. arborum.Numbers in bold indicate the number of OTUs and numbers in italics the relative abundance of the corresponding OTUs in each stage where they are detected. Details of the common OTUs are given in S2 Table.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4596844&req=5

pone.0140014.g003: Venn diagram of bacterial OTUs (at 97% identity) common to the pyrosequencing libraries for eggs (E), L2 larvae (L2) and workers (W) of N. arborum.Numbers in bold indicate the number of OTUs and numbers in italics the relative abundance of the corresponding OTUs in each stage where they are detected. Details of the common OTUs are given in S2 Table.
Mentions: Only two OTUs, accounting for less than 1% in all the pyrotag libraries, were common to the eggs, L2 larvae and worker caste termites of Nasutitermes arborum (Fig 3). These were Bacteroidetes affiliated to the M2PB4-61 Termite group (Rikenellaceae) and the higher termite a cluster (Rs-E47 termite group) respectively (S2 Table). Three OTUs were found in the eggs and L2 larvae and not in workers. They were from the genera Staphylococcus (Staphylococcaceae, Firmicutes), Massilia–6 (Oxalobacteraceae, Betaproteobacteria) and Subcluster Vb (Cluster Vb, Bacteroidetes) and together accounted for about 0.5% of reads in each of these stages. Sixteen OTUs were found in the eggs and worker caste termites but were not found in L2 Larvae. These common OTUs accounted for 6.3% and 18.9% of reads in eggs and workers respectively. They were primarily Firmicutes (5 OTUs, 1.76% or reads from eggs), Actinobacteria (4 OTUs, 2.71%) and Proteobacteria (4 OTUs, 1.39%). 16 OTUs were found in both L2 larvae and workers but not in other stages. There was a higher proportion of these common OTUs in L2 larvae (31.4% of reads), mainly from Bacteroidetes (10 OTUs, 24.36% of reads) especially from the M2PB4-65 termite group, from Treponema Ic cluster of Spirochetes (2 OTUs, 5.78% of reads in L2 larvae) and from Firmicutes (3 OTUs, 0.58% of reads in L2 larvae). These results indicate that there are significantly fewer OTUs in common between developmental stages than OTUs found only in one stage, which represented up to 92.4% of reads (or 70.53% of OTUs) from eggs, 68.4% reads (or 92.92% of OTUs) from L2 larvae, and 74.8% of reads (90.47% of OTUs) from the worker caste.

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Département SOLéO, Institut d'Ecologie et des Sciences de l'Environnement de Paris (IEES), Université Paris Est Créteil (U-PEC), Bâtiment P4, 61 avenue du Général de Gaulle, 94010, Créteil, France.

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.

No MeSH data available.


Related in: MedlinePlus