Evolution and Specificity of a Recently Evolved Chemoautotrophic Ectosymbiosis
Final Report Abstract
Three Niphargus amphipod species from the sulfidic Frasassi caves (central Italy) live in ectosymbioses with sulfur-oxidizing Thiothrix bacteria of three phylogenetic clades: T1, T2 and T3. Whereas T1 and T3 are exclusively associated with Niphargus, free-living counterparts of T2 are found in Frasassi-dwelling microbial mats. The free-living and ectosymbiotic Thiothrix bacteria in Frasassi are exposed to differing redox conditions. One aim of our study was to examine whether the metabolism of T1, T2 and T3 varies according to the distinct ecological niches the bacteria occupy. Incubations with 13C-labeled carbon substrates and 15N nitrogen gas followed by nano-scale Secondary Ion Mass Spectrometry (nanoSIMS) indicated that T2 and T3 ectosymbionts are facultative mixotrophs, while T1 may be heterotrophic. T3 ectosymbionts were further able to fix nitrogen. T2 and T3 ectosymbionts showed differing metabolic traits depending on the Niphargus species they were associated with. Moreover, in the presence of sulfide, autotrophic carbon fixation rates of T2 ectosymbionts of a swimming Niphargus species were significantly higher than those of their free-living counterparts in rock-attaching microbial mats, suggesting that the ectosymbionts derive an ecological advantage from their hitchhiking lifestyle. A second aim was to analyze the genome of the Thiothrix ectosymbionts, focusing on the T2 symbiont of N. ictus. Whereas endosymbiotic genome evolution has been well studied and documented, our study gives the first information concerning genome evolution of ectosymbiotic bacteria. We identified three features of the T2 Thiothrix ectosymbiont genome evolution. First, we observed a high proportion of horizontally transferred genes in the genome, similar to that in genomes of free-living bacteria. Second, the IS transposable elements content is under 3%, as for most bacteria. However, most of the IS copies from our ectosymbiotic strain are degraded and only 5.12% are potentially functional, suggesting a process of genome reduction described previously for endosymbiotic bacteria. Third, the T2 Thiothrix genome has several breakpoints, which could indicate that it maintains several sub-strains on one host in order to survive strongly varying environmental variations in the dynamic Frasassi cave system.
Publications
- (2011). Ectosymbionts of cave-dwelling amphipods: Do different metabolic properties account for host specificity? Gordon Research Conference on Applied and Environmental Microbiology, South Hadley, MA, USA
Bauermeister J, Ionescu D, Dattagupta S
- (2011). Host-specific ectosymbionts of cave-dwelling amphipods: Metabolic ramifications of the symbiotic lifestyle. International Society for Environmental Biogeochemistry (ISEB 20) Conference, Istanbul, Turkey
Dattagupta S, Bauermeister J, Ramette A, Vagner T, Ionescu D, Kuypers, MM
- (2012). Consequences of hitchhiking on metabolic rates of cave amphipod ectosymbionts. Annual Conference of the Association for General and Applied Microbiology, Tübingen, Germany
Bauermeister J§, Ionescu D, Dattagupta S
- (2012). Ecology and evolution of symbioses in cave-dwelling amphipods. GoEvol Symposium, Göttingen, Germany
Dattagupta S, Bauermeister J, Flot J-F
- (2012). Genomic basis and possible evolutionary consequences of ectosymbiotic lifestyle in a sulfide-rich environment. EU COST Action FA0701 Summit meeting, St Pierre d’Oléron, France
Cerveau N§, Bauermeister J and Dattagupta S
- (2012). Metabolic consequences of the “hitchhiking” lifestyle of sulfur-oxidizing ectosymbionts of cave-dwelling amphipods. International Symbiosis Conference (ISS), Krakow, Poland
Dattagupta S, Bauermeister, J, Ionescu, D
- (2012). Repeatedly evolved host-specific ectosymbioses between sulfur-oxidizing bacteria and amphipods living in a cave ecosystem. PLoS ONE 7: e50254
Bauermeister J, Ramette A, Dattagupta S
(See online at https://doi.org/10.1371/journal.pone.0050254) - (2013). Diversity and ecology of ectosymbioses between cave-dwelling amphipods and sulfuroxidizing bacteria. DZG Meeting on Evolutionary Biology, Göttingen, Germany
Bauermeister J, Flot J-F, Dattagupta S
- (2013). Exploring the sulfide tolerance of ectosymbiotic Niphargus amphipods from the Frasassi caves, central Italy. International Journal of Speleology 42(2): 141–145
Bauermeister J, Assig K, Dattagupta S
(See online at https://doi.org/10.5038/1827-806X.42.2.6) - (2013). Genomic basis and possible evolutionary consequences of ectosymbiotic lifestyle in a sulfide-rich environment. XIV Congress of the European Society for Evolutionary Biology (ESEB), Lisbon, Portugal
Cerveau N, Bauermeister J, Dattagupta S
- (2014) Tales from the underground: symbiotic associations of cave-dwelling amphipods. KNVM - Koninklijke Nederlands Vereniging voor Microbiologie Conference, Arnhem, Netherlands
Dattagupta S, Bauermeister J, Flot J-F, Cerveau N, Groeneveld L
- (2014) The Niphargus –Thiothrix ectosymbiosis may be widespread in sulfidic groundwater ecosystems: evidence from Romania. Molecular Ecology. Volume 23, Issue 6, pages 1405–1417
Flot J-F, Bauermeister J, Brad T, Fi er C, Hillebrand A, Sârbu SM, Dattagupta S
(See online at https://doi.org/10.1111/mec.12461)
