Comparative Study of Microbial Biogeochemistry of Devils Hole and Ash Meadows Fish Conservation Facility

Authors: Duane Moser, Joshua Sackett, Brittany Kruger, Scott Hamilton-Brehm

Year: 2018

Abstract

Devils Hole is a tectonic cavern partially filled with deeply sourced groundwater from the Death Valley Regional Flow System (DVRFS). A single skylight in this vast underground system is the sole natural habitat for the critically endangered Devils Hole Pupfish, Cyprinodon diabolis. In Devils Hole, this fish survives under conditions (e.g. high temperatures and low dissolved oxygen concentrations) that would be lethal to most fish. The water of Devils Hole is highly oligotrophic, with extremely low productivity and organic carbon and nutrient concentrations. Like most cave-dominated systems, with the possible exception of the summer when direct sunlight reaches the water surface, the foundations of the food web in Devils Hole are primarily microbial. In the mid-2010s, the Ash Meadows Fish Conservation Facility (AMFCF), a full-scale replica of the uppermost 6.7 m of Devils Hole, was constructed by management agencies to establish a backup population of C. diabolis. To gain a more predictive understanding of the capacity of these unique paired natural and manmade environments to support fish, we evaluated their physical parameters and chemistry in combination with next-generation DNA sequencing of planktonic and benthic bacterial and archaeal communities (16S rRNA gene libraries). Major ion concentrations were consistent between the two systems, but water temperature and dissolved oxygen dynamics differed. Bioavailable nitrogen (primarily nitrate) was 5x lower in AMFCF. Devils Hole and AMFCF nitrogen:phosphorus molar ratios were 107:1 and 22:1, indicative of different nutrient control mechanisms. Both sites possess extraordinarily high microbial diversity, with over 40 prokaryotic phyla represented at each; with 37 shared between them and nearly half deriving from candidate phyla – so-called microbial dark matter lineages. The abundance and composition of predicted photosynthetic primary producers (Cyanobacteria) was markedly different between sites: Devils Hole planktonic and sediment communities were dominated by large and visually conspicuous Oscillatoria spp. (13.2% mean relative abundance), which proved virtually undetectable in AMFCF. Conversely, AMFCF was dominated by a predicted heterotroph from the Verrucomicrobiaceae family (31.7%); which was comparatively rare (<2.4%) in Devils Hole. We propose that the paucity of bioavailable nitrogen in AMFCF, perhaps resulting from physical isolation from allochthonous environmental inputs, is reflected in the microbial assemblage disparity, influences biogeochemical cycling of other dissolved constituents, and may ultimately impact survivorship and recruitment of refuge populations of the Devils Hole Pupfish. This work was dedicated to Lee Simons in a recent publication in PLOS One (Sackett, et al. 2018 13(3):e0194404). Our project was in large measure inspired by conversations with Dr. Simons, who contributed to both its conceptual design and provided insightful comments during preparation of the manuscript. His advocacy and friendship will be missed.