Productivity and Community Composition of Low Biomass/High Silica Precipitation Hot Springs: A Possible Window to Earth's Early Biosphere?

Abstract

Terrestrial hot springs have provided a niche space for microbial communities throughout much of Earth's history, and evidence for hydrothermal deposits on the Martian surface suggest this could have also been the case for the red planet. Prior to the evolution of photosynthesis, life in hot springs on early Earth would have been supported though chemoautotrophy. Today, hot spring geochemical and physical parameters can preclude the occurrence of oxygenic phototrophs, providing an opportunity to characterize the geochemical and microbial components. In the absence of the photo-oxidation of water, chemoautotrophy in these hot springs (and throughout Earth's history) relies on the delivery of exogenous electron acceptors and donors such as H₂, H₂S, and Fe²⁺. Thus, systems fueled by chemoautotrophy are likely energy substrate-limited and support low biomass communities compared to those where oxygenic phototrophs are prevalent. Low biomass silica-precipitating systems have implications for preservation, especially over geologic time. Here, we examine and compare the productivity and composition of low biomass chemoautotrophic versus photoautotrophic communities in silica-saturated hot springs. Our results indicate low biomass chemoautotrophic microbial communities in Yellowstone National Park are supported primarily by sulfur redox reactions and, while similar in total biomass, show higher diversity in anoxygenic phototrophic communities compared to chemoautotrophs. Our data suggest productivity in Archean terrestrial hot springs may be directly linked to redox substrate availability, and there may be high potential for geochemical and physical biosignature preservation from these communities.

Keywords: carbon uptake; early Earth; hot springs; low biomass; silica precipitating.

Figure 1

Map and images of sample site locations. (A) Map showing the hydrothermal areas sampled for this study: IGB = Imperial Geyser Basin of the Lower Geyser Basin, RCA = Rabbit Creek Area of the Midway Geyser Basin, SSA = Sylvan Spring Area of the Gibbon Geyser Basin. Sample site images clockwise from lower left: (B) ‘Heartbeat Pool’, RCA; (C) Closeup of sampling site at ‘Heartbeat Pool’, RCA; (D) ‘Rose Terrace Pool’, RCA; (E) Boulder Geyser with inset of outflow sampling area, IGB; (F) ‘The Dryer’ with inset of sampling area (rock hammer for scale), SSA; (G) ‘Avocado Spring’, SSA with inset of sampling area: grey mat sampled in 2016, red mat sampled in 2018; (H) Dante’s Inferno, SSA; (I) Closeup of sampling site at Dante’s Inferno. Arrows indicate location of sample collection. Scale bars provided in images without visual scale references present. Flow directions for samples collected where flow was occurring: ‘Rose Terrace Pool’—flow is from bottom to upper left; Boulder Geyser outflow (inset)—flow is from left to right; ‘Avocado Spring’—flow is from right to left, and for inset—flow is from left to right.

Figure 2

Carbon uptake experiment results in order (left to right) of increasing pH. L = light dependent (incubated in full light), D = dark treatment (incubated in the dark). Open circles are results of triplicate experiments, bars represent average values with error bars showing standard deviation. Note the difference in y-axis scale for ‘The Dryer’.

Figure 3

Molecular results of sites sampled and carbon uptake experiments conducted, in order (left to right) of increasing pH. Crenarchaeal Orders are presented in the space for the Phylum in the Archaeal sequences bar charts. Remainder = all sequences that account for less than 5% of recovered sequences for all sites. Uncl. = unclassified.

Figure 4

Scanning electron microscope images of sediment samples from ‘Heartbeat Pool’, Midway Geyser Basin, YNP (temperature = 79.2 °C, pH = 3.0). (A) Representative image of sediment textures, (B) inset of ‘A’ highlighting a region with biofilm and Fe-S minerals, (C) zoom in from ‘B’ highlighting physical relationships of mineral particulates (Part.), extracellular polymeric substance (EPS), and iron-sulfide minerals (Fe-S), (D) a separate region of representative sediment textures, (E) a zoom in from ‘D’ highlighting biofilm-mineral physical relationships, and (F) zoom in of ‘E’ showing Part., Fe-S, and EPS associations. All scale bars are 10 µm.

Figure 5

Scanning electron microscope images of sediment samples from Boulder Geyser outflow site, Lower Geyser Basin, YNP (temperature = 84.8 °C, pH = 8.5). (A) Representative image of sediment showing general physical relationships of particulates (Part.), allochthonous diatom frustules (Dia.), and iron-sulfide minerals (Fe-S), (B) image showing silica sheaths that have formed around microbial filaments and associated extracellular polymeric substance (EPS), (C) image highlighting physical relationships of EPS, iron-sulfide minerals (Fe-S), Dia., and silica precipitate (Silica), (D) image highlighting physical relationships between EPS, framboidal Fe-S, and Part., (E) image highlighting colonized Part., Dia., and framboidal and massive Fe-S, and (F) zoom in showing relationship of framboidal Fe-S and EPS from ‘E’. All scale bars are 10 µm.

Figure 6

Scanning electron microscope images of sediment samples from ‘Rose Terrace Pool’, Midway Geyser Basin, YNP (temperature = 74.8 °C, pH = 8.6). (A) Representative image of sediment textures, (B) inset of ‘A’ highlighting a region showing physical relationship of particulates (Part.) and extracellular polymeric substance (EPS) in ‘A’, (C) representative sediment texture with larger Part., (D) inset of ‘C’ highlighting physical relationship of EPS and iron oxide minerals (Fe-oxide), (E) representative sediment texture showing physical relationship of larger particulates and a larger Fe-oxide mineral, and (F) inset of ‘E’ highlighting physical relationship of EPS, Fe-oxides, and Part. All scale bars are 10 µm.

Figure 7

Scanning electron microscope images of sediment samples from Dante’s Inferno, Sylvan Spring Area, Gibbon Geyser Basin, YNP (temperature = 79.4 °C, pH = 5.2). (A) Representative image of sediment textures showing physical relationships of particulates (Part.), elemental sulfur (Sulfur), and iron-sulfides (Fe-S), (B) inset of ‘A’ highlighting a region with Sulfur and Fe-S, (C) zoom in from ‘B’ highlighting physical relationships of Sulfur and EPS, (D) inset from ‘C’ showing the association of EPS surrounding Sulfur and highlighting dissolution/oxidation of Sulfur, (E) inset from ‘B’ highlighting the physical relationship of EPS and Fe-S, and (F) zoom in of ‘E’ showing Fe-S and EPS associations. All scale bars are 10 µm.

Figure 8

Scanning electron microscope images of sediment samples from ‘Avocado Spring’, Sylvan Spring Area, Gibbon Geyser Basin, YNP for left: 2016 (temperature = 69.5 °C, pH = 6.4), and right: 2018 (temperature = 65.6 °C, pH = 6.7). (A) Representative image of mat texture from the 69.5 °C site, (B) inset of ‘A’ highlighting a region with biofilm, (C) zoom in of ‘B’ highlighting physical relationships of mineral particulates (Part.), extracellular polymeric substance (EPS), and iron-sulfide minerals (Fe-S), (D) representative mat texture from the 65.6 °C site, (E) inset from ‘D’ highlighting the physical relationship of Part. and EPS, and (F) inset from ‘D’ highlighting the physical relationship of Fe-S and EPS. All scale bars are 10 µm.

Figure 9

Scanning electron microscope images of sediment samples with an active phototrophic microbial community from ‘The Dryer’, Sylvan Spring Area, Gibbon Geyser Basin, YNP (temperature = 40.5 °C, pH = 7.1). (A) Representative image of surface sediment texture, (B) inset of ‘A’ highlighting a region with biofilm, (C) zoom in of ‘B’ highlighting physical relationships of mineral particulates (Part.) and extracellular polymeric substance (EPS), (D) representative mat texture from a different part of the sample, (E) inset from ‘D’ highlighting a region with silica-encrusted filaments, and (F) inset from ‘E’ highlighting the physical relationship silica sheaths (Silica), Part., and EPS. All scale bars are 10 µm.

Figure 10

Scanning electron microscope images of silica precipitate samples from ‘The Dryer’ showing preserved photosynthetic mat textures, Sylvan Spring Area, Gibbon Geyser Basin, YNP. (A) Representative image of mat texture formed at ‘The Dryer’ during the 2010-2011 mat building period, (B) inset of ‘A’ highlighting the preserved mat and filament textures, (C) zoom in of ‘B’ showing preservation of areas where filaments resided during the active building of the mat textures, (D) representative mat texture from the surface showing the relationship of the active surface with the former mat underneath, (E) inset from ‘D’ highlighting the active surface texture, and (F) inset from ‘E’ highlighting the physical relationship of EPS and Silica. All scale bars are 10 µm.