Fumarole-supported islands of biodiversity within a hyperarid, high-elevation landscape on Socompa Volcano, Puna de Atacama, Andes

Abstract

Fumarolic activity supports the growth of mat-like photoautotrophic communities near the summit (at 6,051 m) of Socompa Volcano in the arid core of the Andes mountains. These communities are isolated within a barren, high-elevation landscape where sparse vascular plants extend to only 4,600 m. Here, we combine biogeochemical and molecular-phylogenetic approaches to characterize the bacterial and eucaryotic assemblages associated with fumarolic and nonfumarolic grounds on Socompa. Small-subunit rRNA genes were PCR amplified, cloned, and sequenced from two fumarolic soil samples and two reference soil samples, including the volcanic debris that covers most of the mountain. The nonfumarolic, dry, volcanic soil was similar in nutrient status to the most extreme Antarctic Dry Valley or Atacama Desert soils, hosted relatively limited microbial communities dominated by Actinobacteria and Fungi, and contained no photoautotrophs. In contrast, modest fumarolic inputs were associated with elevated soil moisture and nutrient levels, the presence of chlorophyll a, and (13)C-rich soil organic carbon. Moreover, this soil hosted diverse photoautotroph-dominated assemblages that contained novel lineages and exhibited structure and composition comparable to those of a wetland near the base of Socompa (3,661-m elevation). Fumarole-associated eucaryotes were particularly diverse, with an abundance of green algal lineages and a novel clade of microarthropods. Our data suggest that volcanic degassing of water and (13)C-rich CO(2) sustains fumarole-associated primary producers, leading to a complex microbial ecosystem within this otherwise barren landscape. Finally, we found that human activities have likely impacted the fumarolic soils and that fumarole-supported photoautotrophic communities may be exceptionally sensitive to anthropogenic disturbance.

FIG. 1.

A map of the south-central Andes mountains and Atacama Desert region showing the location of Socompa Volcano on the border between Argentina and Chile. White areas represent major present-day salt deposits.

FIG. 2.

Socompa sampling locations. (A) Google Earth imagery captured 13 April 2005, 10 days after field collections were made. White arrows indicate sampling locations. Image relief is exaggerated ×2, and background objects are extracted for clarity. The inset image in panel A shows sampling locations as seen from above. (B to D) Photographs of soil-sampling sites. Panel B features the fumarolic ground and mat-like communities described previously as “warmspot 2” by Halloy (22). The inset image in panel B shows the mouth of a rock-tunnel steam vent covered by moss. cf, cold fumarole; wf, warm fumarole; nf, nonfumarole; w, wetland.

FIG. 3.

Broad-level phylogenetic affiliation of Socompa soil SSU rRNA gene sequences. Gray bars show proportions of bacterial phyla (and proteobacterial subphyla), and black bars (inset graphs) show proportions of eucaryotic kingdoms (and fungal phyla) ordered by rank in relative abundance. Numbers of bacterial and eucaryotic sequences, respectively, are 105 and 124 (cold fumarole), 79 and 75 (warm fumarole), 120 and 33 (nonfumarole), and 119 and 45 (wetland). Bacterial-group abbreviations: Acido., Acidobacteria; Actino., Actinobacteria; Alphaprot., Alphaproteobacteria; Bacteroid., Bacteroidetes; Betaprot., Betaproteobacteria; Cyano., Cyanobacteria; Deltaprot., Deltaproteobacteria; Gammaprot., Gammaproteobacteria; Gemmat., Gemmatimonadetes; Plancto., Planctomycetes; Verruco., Verrucomicrobia. AD3, GAL15, OD1, OD2, OP10, OP11, SC3, SC4, SPAM, TM7, WPS-2, WS3, and WS5 are candidate phyla and have no cultured representatives. Eucaryotic-group abbreviations: Alveo., Alveolates; Asco., Ascomycota; Basidio., Basidiomycota; Cerco., Cercozoa; Chytridio., Chytridiomycota; Strameno., Stramenopiles. “Other fungi” are sequences lacking clear affiliation with an established fungal phylum. Libraries also yielded a C1 Crenarchaeota sequence from the cold-fumarole soil and a methanogen-related Euryarchaeota sequence from the wetland soil (not shown).

FIG. 4.

Phylogeny of Verrucomicrobia from Socompa Volcano soils. The Bayesian consensus phylogenetic tree includes 16S rRNA gene sequences from Socompa soils, their closest GenBank BLAST matches, and various representatives of the bacterial phylum Verrucomicrobia. Nodes with <0.50 posterior probability are collapsed. Posterior probabilities for “key” nodes are shown. “Key” nodes generally demonstrate support for affiliation of Socompa soil lineages within established groups. Established subphyla are indicated at the right. Taxon color code is as follows: blue, cold fumarole (cf); red, warm fumarole (wf); yellow, nonfumarole (nf); green, wetland (w); and black, reference taxa with GenBank accession numbers. The scale bar corresponds to 0.10 substitutions per site. Sparto., Spartobacteria; Verruco., Verrucomicrobia; str., strain.

FIG. 5.

Phylogeny of plants and green algae from Socompa Volcano soils. Bayesian consensus tree including 18S rRNA gene sequences from Socompa soils, their closest GenBank BLAST matches, and various representative plant and green-algal taxa. Nodes with <0.50 posterior probability are collapsed. Posterior probabilities for “key” nodes are shown. “Key” nodes generally demonstrate support for affiliation of Socompa soil lineages within established groups. Major groups are shown to the right. Taxon color code is as follows: blue, cold fumarole (cf); green, wetland (w); and black, reference taxa with GenBank accession numbers. Plant and green-algal sequences were not found in warm-fumarole or nonfumarole soils. The scale bar corresponds to 0.10 substitutions per site. The arrow leads to the outgroup. vasc., vascular plants; liver., liverworts; Klebs., Klebsormidiales; gr. alg., green algae.

FIG. 6.

Phylogeny of Metazoa from Socompa Volcano soils. Bayesian consensus tree including 18S rRNA gene sequences from Socompa soils, their closest GenBank BLAST matches, and various representative metazoan taxa. Nodes with <0.50 posterior probability are collapsed. Posterior probabilities for “key” nodes are shown. “Key” nodes generally demonstrate support for affiliation of Socompa soil lineages within established groups. Major groups are shown to the right. Taxon color code is as follows: blue, cold fumarole (cf); green, wetland (w); and black, reference taxa with GenBank accession numbers. Metazoan sequences were not found in warm-fumarole or nonfumarole soils. Reference taxa from the Deuterostomia, Cnidaria, Ctenophora, Porifera, and Lophotrochozoa and the choanoflagellate outgroup were removed for clarity of presentation. The scale bar corresponds to 0.10 substitutions per site. The arrow leads to the outgroup. Arth., Arthropoda; Nem., Nematoda; Rotif., Rotifera; Platy., Platyhelminthes; Gast., Gastrotricha.

FIG. 7.

Collector's curves for Socompa soil bacterial and eucaryotic taxa (OTUs) defined at 99% SSU rRNA gene sequence identity. cf, cold fumarole; wf, warm fumarole; nf, nonfumarole; w, wetland.

FIG. 8.

Phylogenetic richness and evenness within Socompa soil bacterial (A and C) and eucaryotic (B and D) communities. (A and B) PD and the PD gain (G) plotted against soil organic C for each of the four soils. Units of branch length are in the number of substitutions per site (SPS). (C and D) NRI and NTI plotted against soil organic C for each of the four soils. Relatedness indices near zero (dotted line) are considered unstructured (i.e., even). PD, G, NRI, and NTI were each calculated for 100 statistically equivalent phylogenetic trees, and the means are shown. Standard deviations were small and are therefore not shown.

FIG. 9.

Phylogenetic similarity between bacterial (upper dendrogram) and eucaryotic (lower dendrogram) Socompa soil communities. Hierarchically clustered (unweighted-pair group method using average linkages) relationships are based on the unweighted UniFrac metric. Jackknife support for nodes is indicated (1,000 replicates). A distance of zero indicates that the soils contain identical lineages, and a distance of 1 indicates that the soils contain mutually exclusive lineages.