Extremophile at a Glance: Ostracod Crustacean From a Chemoautotrophic Sulphidic Cave Ecosystem

Sulphidic cave ecosystems are remarkable evolutionary hotspots that have witnessed adaptive radiation of their fauna represented by extremophile species having particular traits. Ostracods, a very old group of crustaceans, exhibit specific morphological and ecophysiological features that enable them to thrive in groundwater sulphidic environments. Herein, we report a peculiar new ostracod species Pseudocandona movilaensis sp. nov. thriving in the chemoautotrophic sulphidic groundwater ecosystem of Movile Cave (Romania). The new species displays a set of homoplastic features specific for unrelated stygobitic species, for e.g., triangular carapace in lateral view with reduced postero–dorsal part and simplification of limb chaetotaxy (i.e., loss of some claws and reduction of secondary male sex characteristics), driven by a convergent or parallel evolution during or after colonization of the groundwater realm. P. movilaensis sp. nov. thrives exclusively in sulphidic meso-thermal waters (21°C) with high concentrations of sulphides, methane, and ammonium. Based on the geometric morphometrics-based study of the carapace shape and molecular phylogenetic analyses based on the COI marker (mtDNA), we discuss the phylogenetic relationship and evolutionary implication for the new species to thrive in groundwater sulphidic groundwater environments.

Correction: Brad et al. The Chemoautotrophically Based Movile Cave Groundwater Ecosystem, a Hotspot of Subterranean Biodiversity. Diversity 2021, 13, 128

The authors wish to make the following corrections to this paper [...]

The Chemoautotrophically Based Movile Cave Groundwater Ecosystem, a Hotspot of Subterranean Biodiversity

Movile Cave hosts one of the world’s most diverse subsurface invertebrate communities. In the absence of matter and energy input from the surface, this ecosystem relies entirely on in situ primary productivity by chemoautotrophic microorganisms. The energy source for these microorganisms is the oxidation of hydrogen sulfide provided continuously from the deep thermomineral aquifer, alongside methane, and ammonium. The microbial biofilms that cover the water surface, the cave walls, and the sediments, along with the free-swimming microorganisms, represent the food that protists, rotifers, nematodes, gastropods, and crustacean rely on. Voracious water-scorpions, leeches, and planarians form the peak of the aquatic food web in Movile Cave. The terrestrial community is even more diverse. It is composed of various species of worms, isopods, pseudoscorpions, spiders, centipedes, millipedes, springtails, diplurans, and beetles. An updated list of invertebrate species thriving in Movile Cave is provided herein. With 53 invertebrate species (21 aquatic and 32 terrestrial), of which 38 are endemic for this unusual, but fascinating environment, Movile Cave is the first known chemosynthesis-based groundwater ecosystem. Therefore, Movile Cave deserves stringent attention and protection.

Five million years in the darkness: A new troglomorphic species of Cryptops Leach, 1814 (Chilopoda, Scolopendromorpha) from Movile Cave, Romania

A new species of Cryptops Leach, 1814, C. speleorexsp. nov., is described from Movile Cave, Dobrogea, Romania. The cave is remarkable for its unique ecosystem entirely dependent on methane- and sulfur-oxidising bacteria. Until now, the cave was thought to be inhabited by the epigean species C. anomalans, which is widespread in Europe. Despite its resemblance to C. anomalans, the new species is well-defined morphologically and molecularly based on two mitochondrial (cytochrome c oxidase subunit I COI and 16S rDNA) and one nuclear (28S rDNA) markers. Cryptops speleorex sp. nov. shows a number of troglomorphic traits such as a generally large body and elongated appendages and spiracles, higher number of coxal pores and saw teeth on the tibia of the ultimate leg. With this record, the number of endemic species known from the Movile Cave reaches 35, which ranks it as one of the most species-rich caves in the world.

Genomic and morphologic characterization of a planktonic Thiovulum (Campylobacterota) dominating the surface waters of the sulfidic Movile Cave, Romania

ABSTRACTLife in Movile Cave (Romania) relies entirely on primary carbon fixation by bacteria oxidizing sulfide, methane and ammonia with oxygen, nitrate, sulfate, and ferric iron. There, large spherical-ovoid bacteria (12-16 μm diameter), rich in intracellular sulfur globules, dominate the stable microbial community in the surface water of a hypoxic Air Bell. These were identified as Thiovulum sp. (Campylobacterota). We obtained a closed genome of this Thiovulum and compared it to that of Thiovulum ES. The genes for oxidizing sulfide to sulfate are absent, therefore, Thiovulum likely avoids constant accumulation of elemental sulfur either by oxidizing sulfide to sulfite which is then excreted, or via dissimilatory nitrate reduction to ammonia using the formate-dependent nitrite reductase or hydroxylamine oxidoreductase. Thus, Thiovulum, found also in other caves, is likely important to both S and N cycles in subterranean aquatic ecosystems. Additionally, using electron microscopy, we suggest that in absence of motor-like structures along the membrane, the peritrichous flagella-like structures are type IV pili, for which genes were found in both Thiovulum genomes. These pili may play a role in veil formation, connecting adjacent cells. The force exerted by coordinated movement of such pili may partly explain the exceptionally fast swimming of these bacteria.

A new species of the genus Archiboreoiulus Brolemann, 1921 (Diplopoda, Julida) from Movile Cave (Southern Dobrogea, Romania)

Up to the present, the genus Archiboreoiulus included only two species: A. sollaudi from France and A. pallidus with a wide European distribution range. Here we describe a previously unknown species of the genus Archiboreoiulus, A. serbansarbui, collected from the mesothermal sulfurous Movile Cave, Mangalia, Romania, harboring a rich and diverse troglobitic community.

Comparative genomics analyses indicate differential methylated amine utilisation trait within members of the genusGemmobacter

Methylated amines are ubiquitous in the environment and play a role in regulating the earth’s climate via a set of complex biological and chemical reactions. Microbial degradation of these compounds is thought to be a major sink. Recently we isolated a facultative methylotroph,Gemmobactersp. LW-1, an isolate from the unique environment Movile Cave, Romania, which is capable of methylated amine utilisation as a carbon source. Here, using a comparative genomics approach, we investigate how widespread methylated amine utilisation trait is within the member of the bacterial genusGemmobacter. Five genomes of differentGemmobacterspecies isolated from diverse environments, such as activated sludge, fresh water, sulphuric cave waters (Movile Cave) and the marine environment were available from the public repositories and used for the analysis. Our results indicate that some members of the genusGemmobacter, namelyG. aquatilis, G. caeniandG. sp. LW-1 have the genetic potential of methylated amine utilisation while others (G. megateriumandG. nectariphilus) have not.