Unsuspected diversity of Niphargus amphipods in the chemoautotrophic cave ecosystem of Frasassi, central Italy

Jean-François Flot,Gert Wörheide,Sharmishtha Dattagupta

doi:10.1186/1471-2148-10-171

Jean-François Flot, Gert Wörheide + Show 1 more

Open Access

https://doi.org/10.1186/1471-2148-10-171

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Abstract

BackgroundThe sulfide-rich Frasassi caves in central Italy contain a rare example of a freshwater ecosystem supported entirely by chemoautotrophy. Niphargus ictus, the sole amphipod species previously reported from this locality, was recently shown to host the first known case of a freshwater chemoautotrophic symbiosis. Since the habitat of N. ictus is highly fragmented and is comprised of streams and lakes with various sulfide concentrations, we conducted a detailed study to examine the potential genetic diversity of this species within Frasassi.ResultsBy sequencing one nuclear (ITS) and two mitochondrial (COI and 12S) regions, we show that four partially sympatric Niphargus clades are present in Frasassi. Morphological and behavioral data obtained for three of these clades are perfectly congruent with this molecular delineation and make it possible to distinguish them in the field. Phylogenetic analyses of 28S ribosomal DNA sequences reveal that, among the four clades, only two are closely related to each other. Moreover, these four clades occupy distinct niches that seem to be related to the chemical properties and flow regimes of the various water bodies within Frasassi.ConclusionsOur results suggest that four distinct Niphargus species are present in Frasassi and that they originated from three or four independent invasions of the cave system. At least two among the four species harbor Thiothrix epibionts, which paves the way for further studies of the specificity and evolutionary history of this symbiosis.

Highlights

The sulfide-rich Frasassi caves in central Italy contain a rare example of a freshwater ecosystem supported entirely by chemoautotrophy
Molecular analyses For each marker analyzed (12S, ITS, COI), results obtained using distance, parsimony and likelihood methods were congruent in delimiting four Niphargus clades among our samples (Figures 1, 2 and 3)
Clade 1 comprised 75 individuals collected in five sampling sites in the north-eastern part of the cave complex (Figure 4), Clade 2 grouped 94 samples from all sites except three, Clade 3 comprised 13 specimens from a single location on the northern side of the river (Il Bugianardo), and Clade 4 was represented by only two individuals from one remote site in the south (Lago Primo)

Summary

Introduction

The sulfide-rich Frasassi caves in central Italy contain a rare example of a freshwater ecosystem supported entirely by chemoautotrophy. The sole amphipod species previously reported from this locality, was recently shown to host the first known case of a freshwater chemoautotrophic symbiosis. Amphipods are a major component of the fauna inhabiting these ecosystems [2] and the largest genus among them is Niphargus, which is distributed across most of Europe [3]. Unlike subterranean ecosystems that are fed by aboveground photosynthetic productivity [12], chemoautotrophic caves such as Movile in Romania [13], Frasassi in Italy [14] and Ayyalon in Israel [15] receive their energy input mostly in the form of the chemical hydrogen sulfide arising from underground reservoirs. Animals inhabiting sulfide-rich environments (such as marine sediments [20], hydrothermal vents [21], anchihaline caves [22] and sulfidic caves [23]) face specific metabolic challenges that they counter with avoidance behaviors, adaptations such as sulfide-oxidizing mitochondria and sulfide-binding proteins, or symbioses with sulfide-oxidizing bacteria [24]

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