Tetraponeraants have gut symbionts related to nitrogen–fixing root–nodule bacteria

Abstract

Some Tetraponera ants (Formicidae, Pseudomyrmecinae) subsist almost entirely on amino acid deficient honeydew secretions of pseudococcids and harbour a dense aggregation of bacterial symbionts in a unique pouch-shaped organ at the junction of the midgut and the intestine. The organ is surrounded by a network of intruding tracheae and Malpighian tubules, suggesting that these bacteria are involved in the oxidative recycling of nitrogen-rich metabolic waste. We have examined the ultrastructure of these bacteria and have amplified, cloned and sequenced ribosomal RNA-encoding genes, showing that the ant pouch contains a series of close relatives of Flavobacteria and Rhizobium, Methylobacterium, Burkholderia and Pseudomonas nitrogen-fixing root-nodule bacteria. We argue that pouch bacteria have been repeatedly 'domesticated' by the ants as nitrogen-recycling endosymbionts. This ant-associated community of mutualists is, to our knowledge, the first finding of symbionts related to root-nodule bacteria in animals.

Give us the tools and we will do the job: symbiotic bacteria affect olive fly fitness in a diet-dependent fashion

“…In certain ants of the genus Tetraponera where honeydew has become the main source, if not the sole source, of nutrients, large masses of extracellular bacteria are harboured in a unique pouch in the anterior hindgut (Billen & Buschinger 2000). These bacteria are probably involved in the nutritional enhancement of the ants' diet by recycling nitrogenous waste into amino acid precursors (van Borm et al 2002;Russell et al 2010). Similarly, some Chrysopids (e.g.…”

The interactions of ants with their biotic environment

“…Besides these intracellular endosymbionts, ants have extracellular bacterial endosymbionts in the gut. This has been documented in Tetraponera (Pseudomyrmecinae) ants, which have a dense aggregation of gut bacteria that fix nitrogen and supplement the ants' phloem-based diet [94]. In this special feature, Pringle & Moreau [6] reveal new parts of the endosymbiont puzzle: ants share gut endosymbionts with their hemipteran trophobionts (via the honeydew they feed on).…”

The genome of Rhizobiales bacteria in predatory ants reveals urease gene functions but no genes for nitrogen fixation

“…Blochmannia grows in bacteriocytes in the midgut tissue in carpenter ants and contributes to the nutritional cycle through nitrogen recycling and upgrading of nonessential amino acids123. Likewise, species of tropical arboreal ants (genus Tetraponera ), which feed on nitrogen-poor homopteran exudates, contain gut symbionts related to nitrogen-fixing root-nodule bacteria, which was used to hypothesize a nutritional function via nitrogen fixation4. These ants contain a specialized gut pocket that is enclosed by the trachaea, suggesting that aerial nitrogen may potentially come close enough to the gut to be fixed4.…”

“…Likewise, species of tropical arboreal ants (genus Tetraponera ), which feed on nitrogen-poor homopteran exudates, contain gut symbionts related to nitrogen-fixing root-nodule bacteria, which was used to hypothesize a nutritional function via nitrogen fixation4. These ants contain a specialized gut pocket that is enclosed by the trachaea, suggesting that aerial nitrogen may potentially come close enough to the gut to be fixed4. Consistently, the nifH gene for the dinitrogenase complex was identified in the microbiome of Tetraponera 5, supporting the hypothesis that this capability was the basis for a mutualistic interaction with ants6.…”