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Primary Productivity Below the Seafloor at Deep-Sea Hot Springs

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Primary Productivity Below the Seafloor at Deep-Sea Hot Springs Primary productivity below the seafloor at deep-sea hot springs Jesse McNichola,1,2, Hryhoriy Stryhanyukb, Sean P. Sylvac, François Thomasa,3, Niculina Musatb, Jeffrey S. Seewaldc, and Stefan M. Sieverta,1 aBiology Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543; bDepartment of Isotope Biogeochemistry, Helmholtz Centre for Environmental Research – Umweltforschungszentrum (UFZ), 04318 Leipzig, Germany; and cMarine Chemistry and Geochemistry Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543 Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved May 16, 2018 (received for review March 13, 2018) Below the seafloor at deep-sea hot springs, mixing of geothermal but only one such measurement has been previously obtained under fluids with seawater supports a potentially vast microbial ecosys- realistic temperature and pressure conditions (4). Another im- tem. Although the identity of subseafloor microorganisms is largely portant consideration is that electron acceptors such as oxygen and known, their effect on deep-ocean biogeochemical cycles cannot nitrate rapidly become limiting during incubation experiments with be predicted without quantitative measurements of their meta- vent fluids (13, 14), which may lead to carbon fixation rates being bolic rates and growth efficiency. Here, we report on incubations greatly underestimated (13). However, it is difficult to ascertain the of subseafloor fluids under in situ conditions that quantitatively extent of this bias for existing studies because electron acceptor constrain subseafloor primary productivity, biomass standing stock, consumption has not typically been measured alongside carbon and turnover time. Single-cell-based activity measurements and 16S fixation. Theoretical estimates of primary productivity have also rRNA-gene analysis showed that Campylobacteria dominated car- been derived by combining geochemical measurements with ther- bon fixation and that oxygen concentration and temperature drove modynamic models (15, 16). However, these studies rely on a niche partitioning of closely related phylotypes. Our data reveal a very active subseafloor biosphere that fixes carbon at a rate of up to number of untested assumptions necessary to convert the available −1 −1 energy into biomass. 321 μgC·L ·d , turns over rapidly within tens of hours, rivals the SCIENCES To overcome these limitations, we used a well-studied low- productivity of chemosynthetic symbioses above the seafloor, and ENVIRONMENTAL significantly influences deep-ocean biogeochemical cycling. temperature hot spring known as Crab Spa at the 9°N hydro- thermal vent field on the East Pacific Rise (EPR) as a model deep-sea hydrothermal vents | chemosynthesis | Campylobacteria | ecophysiology | NanoSIMS Significance n 1977, the discovery of deep-sea hot springs revealed unusual The existence of a chemosynthetic subseafloor biosphere was Iecosystems vastly more productive than other regions in the immediately recognized when deep-sea hot springs were dis- energy-limited deep sea (1). This productivity is sustained by covered in 1977. However, quantifying how much new carbon is chemosynthetic microorganisms that harness chemical energy fixed in this environment has remained elusive. In this study, we made available when oxidizing seawater and reducing hydro- incubated natural subseafloor communities under in situ pres- thermal fluid mix. It has long been recognized that the habitat for sure/temperature and measured their chemosynthetic growth such organisms may extend far below the seafloor to vast regions efficiency and metabolic rates. Combining these data with fluid of the ocean crust where fluid mixing takes place (1). Fluids exiting flux and in situ chemical measurements, we derived empirical this subseafloor biosphere are enriched in microbial biomass rel- constraints on chemosynthetic activity in the natural environ- ative to surrounding seawater (2) and contain active microor- ment. Our study shows subseafloor microorganisms are highly ganisms (2–4) that are physiologically and metabolically diverse productive (up to 1.4 Tg C produced yearly), fast-growing – (5–7). Despite the early realization that subseafloor ecosystems (turning over every 17 41 hours), and physiologically diverse. likely contribute significantly to overall chemosynthetic primary These estimates place deep-sea hot springs in a quantitative productivity (1) and provide nutrition to the surrounding food- framework and allow us to assess their importance for global limited deep sea, their extent, productivity, and biological dy- biogeochemical cycles. namics remain poorly constrained (1, 2, 8). It has been generally Author contributions: J.M., J.S.S., and S.M.S. designed research; J.M., H.S., S.P.S., F.T., N.M., assumed that above-seafloor production (i.e., microbe-animal J.S.S., and S.M.S. performed research; N.M., J.S.S., and S.M.S. contributed new reagents/ symbiotic associations) exceeds production below the seafloor analytic tools; J.M., H.S., N.M., J.S.S., and S.M.S. analyzed data; and J.M., J.S.S., and S.M.S. (9). However, this assumption has not been rigorously tested by wrote the paper. empirically quantifying subseafloor productivity. The authors declare no conflict of interest. Quantifying subseafloor productivity at submarine hot springs This article is a PNAS Direct Submission. requires knowledge of both the amount of chemical energy that This open access article is distributed under Creative Commons Attribution-NonCommercial- can be supplied by hydrothermal fluids and the efficiency by NoDerivatives License 4.0 (CC BY-NC-ND). which microbial communities convert this chemical energy into Data deposition: The data reported in this paper have been deposited in the NCBI Se- biomass. Although the chemical composition of hydrothermal quence Read Archive (SRA) (https://www.ncbi.nlm.nih.gov/sra/?term=SRX1898689; acces- sion no. SRX1898689). fluids is well-described and provides strong indirect evidence for 1To whom correspondence may be addressed. Email: [email protected] or ssievert@ high biological activity in the subseafloor (10, 11), the actual whoi.edu. amount of carbon fixed in situ is highly uncertain. Although in 2Present address: University of Southern California, Department of Biological Sciences, Los situ growth yields can be estimated from pure cultures (12), re- Angeles, CA 90089. sults from laboratory cultures may not be relevant to complex 3Present address: Sorbonne Université, CNRS, Integrative Biology of Marine Models and largely uncultivated natural communities growing under (LBI2M), Station Biologique de Roscoff, 29680 Roscoff, France. different physical and chemical conditions. Bulk carbon fixation This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. rates reported for mixed subseafloor microbial communities 1073/pnas.1804351115/-/DCSupplemental. could likewise be used to constrain subseafloor primary productivity, www.pnas.org/cgi/doi/10.1073/pnas.1804351115 PNAS Latest Articles | 1of6 Downloaded by guest on October 2, 2021 Table 1. Predicted versus observed concentrations of potential electron donors and acceptors at Crab Spa + − 2− H2S, μmol/L H2, μmol/L CH4, μmol/L NH4 , μmol/kg O2, μmol/kg NO3 , μmol/L SO4 , mmol/kg Predicted* 552 29 8.1 0.2 107 32 25.8 Observed 184 <2 6.3 11.9 3.6 6.3 26.5 Units are given either per liter or kilogram of Crab Spa vent fluid. *Values are based on fluid mixing calculations previously described in ref. 14. system to constrain subseafloor chemosynthetic production. Microbial Community Composition and Rate Measurements. In all in- Data from incubations conducted under simulated in situ con- cubations, Campylobacteria (7) were the dominant microorganisms, ditions were combined with in situ chemistry and fluid flow rate as shown by catalyzed-reporter deposition fluorescence in situ hy- (14, 17) to arrive at empirical estimates of subseafloor primary bridization (CARD-FISH) cell counts [Fig. 1A and SI Appendix, productivity in a deep-sea hydrothermal system. Table S1;94± 11% of total cells (14)] and the proportion of 16S rRNA gene sequences (97 ± 3.7%; SI Appendix,Fig.S1). Identified Results and Discussion sequences were related to known chemolithoautotrophs, and a Fluids emanating from the subseafloor at Crab Spa are charac- pronounced switch from known mesophilic to thermophilic Cam- terized by a temperature of ∼24 °C, microbial abundances sub- pylobacteria occurred in the incubation at 50 °C (Fig. 1A and SI stantially elevated relative to bottom seawater, and a chemical Appendix,Fig.S1andTableS1). Active carbon fixation was con- 13 − composition for most aqueous species that reflects formation by firmed by specifically measuring H CO3 tracer incorporation in conservative subseafloor mixing of the high-temperature end- campylobacterial cells with halogen in situ hybridization-nanoscale member fluid with seawater (14). Dissolved concentrations of secondary ion mass spectrometry [HISH-SIMS (19); Fig. 2]. HISH- redox reactive sulfide, hydrogen, nitrate, and oxygen, however, are SIMS also demonstrated that amendments increased relative CO2 substantially depleted relative to values expected for conservative fixation rates, especially for oxygen or a combination of nitrate and hydrogen (Fig. 3). Given that Campylobacteria dominate the natural mixing (Table 1), indicating microbial consumption below the ∼ A seafloor (10, 11, 14). Sixteen independent incubation experiments community in sampled
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