Tolerance of flagellated protists to high sulfide and metal concentrations potentially encountered at deep-sea hydrothermal vent

Abstract

The survival rates of 3 species of deep-sea hydrothermal vent flagellates were measured after exposure to chemical conditions potentially encountered in vent environments. The survival rates, measured as viability through time, of Caecitellus parvulus, Cafeteria sp. and Rhynchomonas nasuta were determined and compared to shallow-water strains of the same species after exposure to increasing concentrations of sulfide or the metals Cu, Fe, Mn and Zn. Responses were variable but in all cases these flagellates showed very high tolerance to extreme conditions. Cafeteria spp. were remarkable in that both strains showed 100% viability after a 24 h exposure to 30 mM sulfide under anoxic conditions. By contrast, the highest naturally occurring sulfide concentrations ever measured are only 18 to 20 mM. There was little effect from metals at concentrations up to 10 -3 M total metal, but a sharp decrease in viability occurred between 10 -3 and 10 -2 M total metal, due either to a rapid increase in the availability of free metal ions or colloid formation or both. This study is consistent with other previously reported studies that indicate these flagellate species are present and capable of being active members of the microbial food webs at deep-sea vents. KEY WORDS:Flagellate · Survival · Hydrogen sulfide · Metals · Hydrothermal vent · Extreme environment 226: 63-75, 2002 Hydrothermal vents are comprised of some of the most extreme environments on Earth. Vent fluids are hotter, more acidic and enriched with metals and dissolved gasses than the surrounding seawater (Table 1). Characterized by very steep physical and chemical gradients between vent fluids and seawater, vent fields may rival the abiotic environments characteristic of other planets. Still, life occurs at vents in abundance. The question remains as to how some organisms, particularly cosmopolitan species, are able to tolerate and survive under vent conditions. This is especially true for microorganisms like the flagellated protists that arrive in the deep sea on sinking particulate matter (Silver & Alldredge 1981, Patterson & Fenchel 1990 and have been shown to be members of deep-sea benthos (Burnett 1977, Turley et al. 1988) and deep-sea vent microenvironments (Atkins et al. 1998(Atkins et al. , 2000. Resale or republication not permitted without written consent of the publisherMar Ecol Prog SerThe present study determined the effects of both sulfide (H 2 S, HS -and S 2 -) and metals, at concentrations approaching those found in end-member fluids emanating from deep-sea hydrothermal vents, on ubiquitous species of flagellates isolated from these environments. End-member vent fluid concentrations of transition metal species are enriched several orders of magnitude relative to average seawater (Seyfried & Mottl 1995), and sulfide concentrations may reach several millimolar (Table 1). Among protists, sulfide tolerance has been studied mostly in ciliates from natural environments with concentrations much lower than vent fluids (Bick & Kunze 1971, Matsu...

Identity of epibiotic bacteria on symbiontid euglenozoans in O2-depleted marine sediments: evidence for symbiont and host co-evolution

“…concentrations of hydrogen sulfide (up to 30 mM (Atkins et al, 2002)), which together with the recent diversity data supports the idea that protists form important components of microbial communities in anoxic, oxygen-depleted and/or sulfidic marine environments. What is intriguing is that, hydrogen sulfide at micromolar concentrations is known to inhibit respiration and, therefore, the otherwise aerobic eukaryotes in these environments must have physiological adaptations that allow them to survive.…”

Sulfide Ameliorates Metal Toxicity for Deep-Sea Hydrothermal Vent Archaea

“…Similarly, the chemical speciation of metals as metalsulfide complexes may be important for the survival of archaeal communities at deep-sea hydrothermal vents. The ability of hydrothermal vent archaea to survive extreme metal concentrations may not be due solely to a physiological or genetic capability (26) as has been suggested for protists at vent sites (2). Additionally, metal-sulfide complex formation acts as a chemical defense mechanism that buffers the concentration of bioavailable metals before physiological detoxification reactions set in.…”

“…For each metal studied, sulfide forms dissolved complexes with divalent metal cations [equation 1; note that metal-sulfide complexes have numerous stoichiometries, e.g., MHS ϩ , M(HS) 2 , and M 2 S 3 ] (17, 23) until the solubility product (K sp ) is exceeded (equation 2):…”

“…c Zinc-free ion concentrations are calculated at room temperature by using stability constants for ZnS and Zn(HS) 2 (17,31) and for chloro complexes (NIST database [see above]). In parentheses, zinc-free ion concentrations are calculated by using stability constants determined at 100°C (3) for Zn chloro complexes and Zn(HS) 2 and Zn(HS) 3 Ϫ . The differences in results between temperatures are due to incomplete stability constant data for higher temperatures as well as more sensitive voltammetric methods for determining stability constants at room temperature.…”

Growth and Grazing Kinetics of the Facultative Anaerobic Nanoflagellate, <i>Suigetsumonas clinomigrationis</i>

“…Heterotrophic nanoflagellates (HNF) are important bacterial consumers in the microbial loop (17, 23). HNF have also been detected in the anoxic bottom waters of stratified lakes (11, 18, 21) and in anaerobic cultures from anoxic habitats (3) and deep-sea hydrothermal vents (1). However, HNF ecology in anoxic environments currently remains unclear because of limited data on the abundance and bacterivory of HNF under these conditions (18, 22).…”