Abstract
Ectosymbioses between invertebrates and sulfur-oxidizing bacteria are widespread in sulfidic marine environments and have evolved independently in several invertebrate phyla. The first example from a freshwater habitat, involving Niphargus ictus amphipods and filamentous Thiothrix ectosymbionts, was recently reported from the sulfide-rich Frasassi caves in Italy. Subsequently, two new Niphargus species, N. frasassianus and N. montanarius, were discovered within Frasassi and found to co-occur with N. ictus. Using a variety of microscopic and molecular techniques, we found that all three Frasassi-dwelling Niphargus species harbor Thiothrix ectosymbionts, which belong to three distinct phylogenetic clades (named T1, T2, and T3). T1 and T3 Thiothrix dominate the N. frasassianus ectosymbiont community, whereas T2 and T3 are prevalent on N. ictus and N. montanarius. Relative distribution patterns of the three ectosymbionts are host species-specific and consistent over different sampling locations and collection years. Free-living counterparts of T1–T3 are rare or absent in Frasassi cave microbial mats, suggesting that ectosymbiont transmission among Niphargus occurs primarily through inter- or intraspecific inoculations. Phylogenetic analyses indicate that the Niphargus-Thiothrix association has evolved independently at least two times. While ectosymbioses with T1 and T2 may have been established within Frasassi, T3 ectosymbionts seem to have been introduced to the cave system by Niphargus.
Highlights
Symbioses are vital for virtually all living organisms
Scanning Electron Microscopy (SEM) examination revealed that individuals of all three Niphargus species harbored filamentous bacteria which were attached via holdfasts to hairs and spines on the hosts’ legs and antennae (Figure 3)
While both examined N. frasassianus specimens and the only inspected N. montanarius individual harbored abundant, long bacterial filaments often arranged in rosettes (Figure 3, panels A and C), three out of nine investigated N. ictus individuals carried only very few, solitary filaments
Summary
Symbioses are vital for virtually all living organisms. They were critical for the origin and diversification of Eukaryotes and remain a major driving force in evolution, as they induce diverse physiological, morphological, and developmental modifications in the species involved [1]. The animals are exposed to diverse free-living microbial communities and susceptible to colonization by many opportunistic, non-specific surface-dwellers [4], many of them have established long-term and specific relationships with only few selected sulfur-oxidizing bacteria [5,6,7,8,9,10]. Most of these ectosymbionts belong to distinct groups within the epsilon- and gammaproteobacterial subdivisions. Bacteria within the families Thiovulgaceae and Thiotrichaceae seem to have evolved an enhanced ability to establish ectosymbioses [3]
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