Microbial eukaryotic predation pressure and biomass at deep-sea hydrothermal vents

Abstract

Deep-sea hydrothermal vent geochemistry shapes the foundation of the microbial food web by fueling chemolithoautotrophic microbial activity. Microbial eukaryotes (or protists) play a critical role in hydrothermal vent food webs as consumers and hosts of symbiotic bacteria, and as a nutritional source to higher trophic levels. We measured microbial eukaryotic cell abundance and predation pressure in low-temperature diffuse hydrothermal fluids at the Von Damm and Piccard vent fields along the Mid-Cayman Rise in the Western Caribbean Sea. We present findings from experiments performed under in situ pressure that show cell abundances and grazing rates higher than those done at 1 atmosphere (shipboard ambient pressure); this trend was attributed to the impact of depressurization on cell integrity. A relationship between the protistan grazing rate, prey cell abundance, and temperature of end-member hydrothermal vent fluid was observed at both vent fields, regardless of experimental approach. Our results show substantial protistan biomass at hydrothermally fueled microbial food webs, and when coupled with improved grazing estimates, suggest an important contribution of grazers to the local carbon export and supply of nutrient resources to the deep ocean.

Keywords: deep-sea food web ecology; deep-sea hydrothermal vents; microbial eukaryotes; predator–prey interactions; protists.

Graphical Abstract

Figure 1

Eukaryotic cell abundance (a and b) and grazing (c and d) results from the Mid-Cayman Rise. Each boxplot outlines the first and third quartiles (lower and upper hinges of the box), and the thicker line in the middle corresponds to the median. Whiskers extending beyond each box show the range of the smallest and largest values. Boxplots are overlaid with the actual values for cell abundances and grazing rates, which are also listed in Table 1. (a) Comparison of eukaryote cells ml⁻¹ (log scale) at time zero (Tf) by vent field (Von Damm at left; Piccard at right) and vent habitat type, where vent includes results from all sites of active diffuse flow and non-vent includes plume and deep background seawater. (b) Cell abundances from each vent site are also shown by experimental approach, where shipboard denotes results from grazing experiments conducted at ambient pressure and IGT corresponds to experiments run at in situ pressure. (c) Protistan grazing rates across each vent field and vent versus non-vent environments. Results are expressed as the number of cells consumed by protistan predators ml⁻¹ hr⁻¹ (log scale). (d) Grazing experiment results from vent sites only are shown again, but grouped by experimental approach (shipboard versus IGT). Symbol color denotes vent field (black symbols in B and D include both Von Damm and Piccard), filled-in circles are derived from shipboard experiments or samples (ambient pressure), and circle outlines represent results from IGT experiments (in situ pressure).

Figure 2

Grazing rates (cells consumed ml⁻¹ hr⁻¹), along the x-axis, are shown with (a) eukaryote cells ml⁻¹ and (b) prokaryote cells ml⁻¹ along the y-axes. Symbol color denotes the temperature of fluid at time of sample collection (°C). Filled in triangle symbols are derived from shipboard experiments conducted at ambient pressure, while triangle outlines represent results from IGT experiments performed under in situ pressure. Error bars represent the standard mean error for the cell counts (y-axes) or grazing rate (x-axis). All values are also reported in Table 1.

Figure 3

(a) Ordination analysis based on 18S rRNA gene amplicon sequencing. Samples include the in situ microbial eukaryotic community (open triangle symbols) and the Tf for grazing incubations conducted at ambient pressure (filled-in triangle symbols). No molecular samples were available from the IGT grazing experiments. Before PCA analysis, data were center-log ratio transformed. The x and y axes represent 12.3% and 9.7% of the variability among samples, respectively. Color designates each vent site, plume, or background sample and symbol differentiates the vent field. (b) Output from corncob analysis [33], which identified specific families that may be enriched within vent samples (positive coefficient) compared to non-vent samples (negative coefficient; includes background and plume).

Figure 4

Schematic of the microbial food web at the Mid-Cayman Rise hydrothermal vent fields in terms of carbon. Rates are expressed as μg C L⁻¹ day⁻¹ (dashed line boxes) and biomass is represented by μg C L⁻¹ (solid line boxes). Values are derived from experiments conducted with diffuse flow vent fluid and list the reported average (bolded), minimum, and maximum (parenthetical). Arrows show the net flow of carbon to higher trophic levels and unconstrained losses. In order to show results alongside primary production, we included the range of chemosynthetic primary production derived from McNichol et al. [33]. Eukaryote and prokaryote biomass was determined by multiplying carbon conversion factors by cell abundances from this study (see Table 2 for equations). Protistan grazing rate was calculated by converting predation rate into μg of carbon (see Tables 3 and 4). Image created with BioRender.com.