Prokaryotic communities from a lava tube cave in La Palma Island (Spain) are involved in the biogeochemical cycle of major elements

Abstract

Lava caves differ from karstic caves in their genesis and mineral composition. Subsurface microbiology of lava tube caves in Canary Islands, a volcanic archipelago in the Atlantic Ocean, is largely unknown. We have focused the investigation in a representative lava tube cave, Fuente de la Canaria Cave, in La Palma Island, Spain, which presents different types of speleothems and colored microbial mats. Four samples collected in this cave were studied using DNA next-generation sequencing and field emission scanning electron microscopy for bacterial identification, functional profiling, and morphological characterization. The data showed an almost exclusive dominance of Bacteria over Archaea. The distribution in phyla revealed a majority abundance of Proteobacteria (37-89%), followed by Actinobacteria, Acidobacteria and Candidatus Rokubacteria. These four phyla comprised a total relative abundance of 72-96%. The main ecological functions in the microbial communities were chemoheterotrophy, methanotrophy, sulfur and nitrogen metabolisms, and CO₂ fixation; although other ecological functions were outlined. Genome annotations of the especially representative taxon Ga0077536 (about 71% of abundance in moonmilk) predicted the presence of genes involved in CO₂ fixation, formaldehyde consumption, sulfur and nitrogen metabolisms, and microbially-induced carbonate precipitation. The detection of several putative lineages associated with C, N, S, Fe and Mn indicates that Fuente de la Canaria Cave basalts are colonized by metabolically diverse prokaryotic communities involved in the biogeochemical cycling of major elements.

Keywords: Biogeochemical cycles; La Palma Island; Lava tube; Proteobacteria; Volcanic cave.

Figure 1. Map of Fuente de la Canaria Cave, La Palma Island.

Planimetry and cross-section of Fuente de la Canaria Cave.

Figure 2. Samples collected from Fuente de la Canaria Cave.

Field images of the mineral deposits and colored microbial colonies collected from Fuente de la Canaria Cave (MZ03) in La Palma Island (Spain). (A) sample MZ03-2B. (B) sample MZ03-3C. (C) sample MZ03-8H. (D) sample MZ03-10J.

Figure 3. Field Emission Scanning Electron Microscopy images of samples.

Representative Field Emission Scanning Electron Microscopy images of the studied samples, depicting (A,B) Clusters of Actinobacteria-like cells with spiny surface ornamentation in the mucous formation of ochre color (MZ03-2B); (C) Microbial filaments probably of Actinobacteria in the ochre soft stalactite (MZ03-3C); (D) Hollow bacterial filament on the sample surface of the ochre soft stalactite (MZ03-3C); (E) Prosthecate-like bacterial cell in the ochre mucous deposit on a rock crack with water runoff (MZ03-8H); (F) Dense network of nano-scaled filaments in the ochre mucous deposit on a rock crack with water runoff (MZ03-8H); (G) Mass of interwoven filaments, and (H) Coccoid-shaped cells with smooth surfaces in the mineral formation with abundant moonmilk deposits (MZ03-10J).

Figure 4. Taxonomic identifications of Bacteria at class level.

Heat-map analysis of Fuente de la Canaria Cave with taxonomic identifications of Bacteria at class level. The classes are described in the right column and their respective abundances included in the boxes. Colored left bar groups the classification at phylum level.

Figure 5. Taxonomic identifications of Bacteria at family/genus level.

Heat-map analysis of Fuente de la Canaria Cave with taxonomic identifications of Bacteria at family/genus level. The families/genera are described in the right column and their respective abundances included in the boxes. Colored left bar groups the classification at order level.

Figure 6. Predicted ecological functions of Bacteria.

Relative abundance of FAPROTAX predicted ecological functions (Y axis) of Fuente de la Canaria Cave. The size of the cycles indicates the relative abundance.

Figure 7. Predicted genes encoding enzymes.

Heat-map showing the relative abundances of PICRUSt2 predicted genes (Y axis) encoding the enzymes involved in methane, sulfur, nitrogen metabolism and CO₂ fixation based on Metacyc database for each sampling point (X axis). The values for functional groups are marked by colors from white to red designating the least abundant to most abundant.