Geochemical Constraints on Potential Biomass Sustained by Subseafloor Water–Rock Interactions

Abstract

Since the first discovery of macrofaunal and microbial communities endemic to hydrothermal vents, chemolithoautotrophic microorganisms at and beneath the seafloor have attracted the interest of many researchers. This type of microorganism is known to obtain energy from inorganic substances (e.g., reduced sulfur compounds, molecular hydrogen, and methane) derived from subsurface physical and chemical processes, such as water-rock interactions. As the primary producers, they sustain chemosynthetic ecosystems, which are fundamentally different from terrestrial and shallow marine ecosystems that are sustained by photosynthetic primary production. It is possible that the chemosynthetic ecosystems at and beneath the seafloor are vast and metabolically active, playing an important role in the global geochemical cycles of many bio-essential elements. However, even today, the spatial and temporal distributions of the unseen chemosynthetic biosphere are largely uncertain. Here, we present geochemical constraints on the estimate of the potential biomass in seafloor and subseafloor chemosynthetic ecosystems sustained by high-temperature deep-sea hydrothermal activities and low-temperature alteration/weathering of oceanic crust. The calculations are based on the fluxes of metabolic energy sources (S, H 2 , Fe, and CH 4 ), the chemical energy yields for metabolic reactions, and the maintenance energy requirements. The results show that for deep-sea hydrothermal vent ecosystems, most bioavailable energy yields (86 %) are due to oxidation reactions of S. In contrast, for subseafloor oceanic crust ecosystems, oxidation reactions of Fe and S generally yield the same amounts of bioavailable energy (59 % and 41 %, respectively). The estimated biomass potential in the subseafloor oceanic crust ecosystems (0.14 Pg C) is one order of magnitude higher than that in global deep-sea hydrothermal vent ecosystems (0.0074 Pg C), most likely reflecting the greater flux of

Inactive Sulfide Ecosystems in the Deep Sea: A Review

“…Microbiologists were first motivated to study microbial communities on metal sulfides (Wirsen et al, 1993;Edwards et al, 2003a) because morphological characteristics of the feeding appendages and gut contents of the dominant invertebrate (shrimp) at the TAG hydrothermal site on the Mid-Atlantic Ridge suggested ingestion of a microbially enriched substratum (Van Dover et al, 1988). An early account of pyrite (FeS 2 )associated chemolithoautotrophic microbes that oxidize sulfide noted that polymetallic sulfides can serve as a "stable source of electrons for chemosynthetic production of organic carbon in the deep sea" long after hydrothermal activity ceases (Eberhard et al, 1995), a point that has since been underscored by others (McCollom, 2000;Edwards, 2004;Edwards et al, 2005;Nakamura and Takai, 2015;Kato and Yamagishi, 2016).…”

Primary productivity below the seafloor at deep-sea hot springs

“…However, it is difficult to ascertain the extent of this bias for existing studies because electron acceptor consumption has not typically been measured alongside carbon fixation. Theoretical estimates of primary productivity have also been derived by combining geochemical measurements with thermodynamic models ( 15 , 16 ). However, these studies rely on a number of untested assumptions necessary to convert the available energy into biomass.…”

Productivity, metabolism and physiology of free-living chemoautotrophic Epsilonproteobacteria

“…We also calculated a minimum global standing stock of 1.4 2.7 × 10 9 g C, three orders of magnitude lower than 7.4 × 10 12 g C estimated from a thermodynamic framework (Nakamura and Takai, 2015). Our standing stock represents a minimum value; if percell rates in situ were slower, or if cell-specific rates were similar but carbon per cell was higher, our estimate would increase.…”

“…In contrast, previous studies have used thermodynamic calculations to estimate total bioavailable energy and used this data to estimate primary productivity in situ. However, these studies have relied on assumptions to either convert energy to ATP and subsequently biomass (McCollom and Shock, 1997) or have used values for cellular maintenance energy to estimate total biomass standing stock (Nakamura and Takai, 2015). However, these assumptions are have not been rigorously tested with hydrothermal vent communities or isolates.…”

“…Our standing stock represents a minimum value; if percell rates in situ were slower, or if cell-specific rates were similar but carbon per cell was higher, our estimate would increase. In Nakamura and Takai (2015), the authors assumed a maintenance energy for non-growing cells to calculate the standing stock biomass, which 2 See methods for details is not realistic based on our results showing microbes are active and grow rapidly.…”