Microbial ecology of serpentinite-hosted ecosystems

Abstract

Serpentinization, the collective set of geochemical reactions initiated by the hydration of ultramafic rock, has occurred throughout Earth history and is inferred to occur on several planets and moons in our solar system. These reactions generate highly reducing conditions that can drive organic synthesis reactions potentially conducive to the emergence of life, while concomitantly generating fluids that challenge life owing to hyperalkalinity and limited inorganic carbon (and oxidant) availability. Consequently, the serpentinite-hosted biosphere offers insights into the earliest life, the habitable limits for life, and the potential for life on other planets. However, the support of abundant microbial communities by serpentinites was only recognized ~20 years ago with the discovery of deep-sea hydrothermal vents emanating serpentinized fluids. Here, we review the microbial ecology of both marine and continental serpentinization-influenced ecosystems in conjunction with a comparison of publicly available metagenomic sequence data from these communities to provide a global perspective of serpentinite microbial ecology. Synthesis of observations across global systems reveal consistent themes in the diversity, ecology, and functioning of communities. Nevertheless, individual systems exhibit nuances due to local geology, hydrology, and input of oxidized, near-surface/seawater fluids. Further, several new (and old) questions remain including the provenance of carbon to support biomass synthesis, the physical and chemical limits of life in serpentinites, the mode and tempo of in situ evolution, and the extent that modern serpentinites serve as analogs for those on early Earth. These topics are explored from a microbial perspective to outline key knowledge-gaps for future research.

Keywords: Serpentinite; acetogens; astrobiology; carbon fixation; early earth; hydrogen; hydrogenase; methanogens; microbial ecology.

Fig. 1

Global distribution of serpentinization-influenced environments that have been investigated microbiologically and those that hosted 70 publicly available shotgun metagenomes used in the meta-analysis of this review. Geologic systems are indicated by points and abbreviations on the map, with those in green hosting metagenomes that were used in the meta-analysis of this review. Bottom left insert shows the pH distribution of water samples from which the metagenomes were derived, as reported by the original publication. Additional information for metagenomes is shown in Supplementary Table 1. Abbreviations are defined as follows (and further identified in Supplementary Table 1). NEY: Ney Springs; CED: The Cedars; CROMO: Coast Range Ophiolite Microbial Observatory; SEO: Santa Elena Ophiolite; TBL: Tablelands Ophiolite; RHF: Rainbow Hydrothermal Field; LCHF: Lost City Hydrothermal Field; LVF: Logatchev Vent Field; AVF: Ashadze Vent Field; AUR: Aurora Seamount; LEKA: Leka Ophiolite; CDV: Cabeço de Vide; VOL: Voltri Massif; YAN: Yanartaş; ALL: Allas Springs; SAM: Samail Ophiolite; KMR: Khalilovsky Massif; KHF: Karei Hydrothermal Field; OCHF: Old City Hydrothermal Field; HHS: Hakuba Happo Hot Springs; MAN: Manleluag Spring; LCR: La Crouen Spring; PBHF: Prony Bay Hydrothermal Field.

Fig. 2

Taxonomic composition of 70 community metagenomes from serpentinization-influenced environments. Each row represents a metagenome organized by site and by increasing pH from top to bottom (within each site). Each column represents a taxonomic group that was identified in >1% relative abundance in at least one of the metagenomes. Metagenomic data and publicly available accession information is provided in Supplementary Table 1. Community composition was evaluated from raw reads using the SingleM pipeline (described in Supplementary Methods). Taxonomic groups are defined as in the genome tree database (GTDB) at various taxonomic levels: p: Phylum; c: Class; o: Order; f: Family; g: Genus. Sub-phylum level taxa that are discussed in the manuscript are specifically included. Circles are colored by their corresponding system and sized according to their estimated relative abundance, as indicated by the legend on the bottom left.

Figure 3

Variation in the composition and abundance of hydrogenase enzyme homologs encoded among 68 publicly available community metagenomes from serpentinization-influenced environments. a) Non-metric multidimensional scaling (NMDS) ordination of the hydrogenase profiles among 68 metagenomes, as predicted using the METABOLIC platform (described in supplementary methods). Points are colored according to the pH of the environment from where the metagenome derives, as indicated by the scale to the right. b) the total fraction of all hydrogenase orthologs relative to the total encoded proteins of a metagenome. Points are shown in relation to the pH of the environment from where the metagenome derives, with the system of origin indicated by color.

Figure 4

Metagenomic and taxonomic diversity of 70 publicly available community metagenomes from serpentinization-influenced environments. a) Metagenomic diversity, as measured by the Nonpareil diversity metric, plotted as a function of the pH of the environment where the metagenome derives (linear regression R²_adj = 0.25, P ≤ 0.0001). Points are colored by system of origin. b and c) non-metric multidimensional scaling ordinations based on dissimilarity in the taxonomic profiles among communities, as evaluated with assembly-free analysis with the SingleM package (described in Supplementary Methods). Points are colored by their system of origin (b) as indicated in panel a, or by the pH of their sample based on the color scale to the right (c). Two samples did not have corresponding reported pH values and are shown as white circles. System of origin (b) was significantly associated with compositional variation based on envfit analysis (R² = 0.56, P < 0.00), whereas pH (c) was only marginally associated with compositional variation (R² = 0.09, P = 0.04). Additional sample information is provided in Supplementary Table 1.

Figure 5

Variation in metabolic functional potential among 68 publicly available community metagenomes from serpentinization-influenced environments. a) Non-metric multidimensional scaling (NMDS) ordination of the functional potential profiles among 68 metagenomes (described in Supplementary Methods). Points are colored by (a) their system of origin, as indicated by the legend on the bottom right and (b) the pH of their sample, based on the color scale to the right. Two samples did not have corresponding reported pH values and are shown as white circles. System of origin (a) was significantly associated with compositional variation based on envfit analysis (R² = 0.54, P ≤ 0.001), and pH (b) was also associated with compositional variation, but to a lesser extent (R² = 0.25, P ≤ 0.001). Additional sample information is provided in Supplementary Table 1.

Figure 6

Phylogenetic reconstruction of major archaeal lineages highlighting those that are abundant in serpentinite systems. The tree was modified from the maximum likelihood phylogeny of archaeal orders described in Mei et al. 2023. The newick tree corresponding to Fig. 1a in the above study was used to highlight taxonomic lineages discussed in this review. Cohesive clades that coincided with taxonomic classifications are collapsed and shown as triangles, with those in blue corresponding to taxa that have been identified in serpentinite ecosystems and that are discussed in the main text. Notable taxa found in serpentinite communities are indicated after the forward slash and are in italics. The tree was rooted with bacterial taxa (not shown). Scale shows expected number of substitutions / site.

Figure 7

Phylogenetic reconstruction of major bacterial lineages highlighting those that are abundant in serpentinite systems. The tree was modified from the maximum likelihood phylogeny of bacterial orders described in Martinez-Gutierrez et al. 2021 (described in Supplementary Methods). Cohesive clades that coincided with taxonomic classifications are collapsed and shown as triangles, with those in blue corresponding to taxa that have been identified in serpentinite ecosystems and that are discussed in the main text. Notable taxa found in serpentinite communities are indicated after the forward slash and in italics. The tree was rooted with archaeal taxa (not shown). Scale shows expected number of substitutions / site.