Seafloor Incubation Experiment with Deep-Sea Hydrothermal Vent Fluid Reveals Effect of Pressure and Lag Time on Autotrophic Microbial Communities
Open Access
- 1 May 2021
- journal article
- research article
- Published by American Society for Microbiology in Applied and Environmental Microbiology
- Vol. 87 (9)
- https://doi.org/10.1128/AEM.00078-21
Abstract
Depressurization and sample processing delays may impact the outcome of shipboard microbial incubations of samples collected from the deep sea. To address this knowledge gap, we developed a remotely operated vehicle (ROV)-powered incubator instrument to carry out and compare results from in situ and shipboard RNA stable isotope probing (RNA-SIP) experiments to identify the key chemolithoautotrophic microbes and metabolisms in diffuse, low-temperature venting fluids from Axial Seamount. All the incubations showed microbial uptake of labeled bicarbonate primarily by thermophilic autotrophic Epsilonbacteraeota that oxidized hydrogen coupled with nitrate reduction. However, the in situ seafloor incubations showed higher abundances of transcripts annotated for aerobic processes, suggesting that oxygen was lost from the hydrothermal fluid samples prior to shipboard analysis. Furthermore, transcripts for thermal stress proteins such as heat shock chaperones and proteases were significantly more abundant in the shipboard incubations, suggesting that depressurization induced thermal stress in the metabolically active microbes in these incubations. Together, the results indicate that while the autotrophic microbial communities in the shipboard and seafloor experiments behaved similarly, there were distinct differences that provide new insight into the activities of natural microbial assemblages under nearly native conditions in the ocean. IMPORTANCE Diverse microbial communities drive biogeochemical cycles in Earth's ocean, yet studying these organisms and processes is often limited by technological capabilities, especially in the deep ocean. In this study, we used a novel marine microbial incubator instrument capable of in situ experimentation to investigate microbial primary producers at deep-sea hydrothermal vents. We carried out identical stable isotope probing experiments coupled to RNA sequencing both on the seafloor and on the ship to examine thermophilic, microbial autotrophs in venting fluids from an active submarine volcano. Our results indicate that microbial communities were significantly impacted by the effects of depressurization and sample processing delays, with shipboard microbial communities being more stressed than seafloor incubations. Differences in metabolism were also apparent and are likely linked to the chemistry of the fluid at the beginning of the experiment. Microbial experimentation in the natural habitat provides new insights into understanding microbial activities in the ocean.Funding Information
- Gordon and Betty Moore Foundation (GBMF3297)
- National Science Foundation (OCE-0939564)
- National Science Foundation (OCE-1546695)
- National Science Foundation (OCE-1547004)
- Schmidt Ocean Institute (FK010-2013)
This publication has 58 references indexed in Scilit:
- Autonomous Application of Quantitative PCR in the Deep Sea: In Situ Surveys of Aerobic Methanotrophs Using the Deep-Sea Environmental Sample ProcessorEnvironmental Science & Technology, 2013
- Experimental Incubations Elicit Profound Changes in Community Transcription in OMZ BacterioplanktonPLOS ONE, 2012
- Fast gapped-read alignment with Bowtie 2Nature Methods, 2012
- Chemoautotrophy at Deep-Sea Vents: Past, Present, and FutureOceanography, 2012
- Nautilia nitratireducens sp. nov., a thermophilic, anaerobic, chemosynthetic, nitrate-ammonifying bacterium isolated from a deep-sea hydrothermal ventInternational Journal of Systematic and Evolutionary Microbiology, 2010
- Individual hydrothermal vents at Axial Seamount harbor distinct subseafloor microbial communitiesFEMS Microbiology Ecology, 2009
- Short‐term microbial and physico‐chemical variability in low‐temperature hydrothermal fluids near 5°S on the Mid‐Atlantic RidgeEnvironmental Microbiology, 2009
- The Sequence Alignment/Map format and SAMtoolsBioinformatics, 2009
- GroES/GroEL and DnaK/DnaJ Have Distinct Roles in Stress Responses and during Cell Cycle Progression inCaulobacter crescentusJournal of Bacteriology, 2006
- Instrumentation for the measurement of phytoplankton production1Limnology and Oceanography, 1983