Probing the Depths of Life

May 24, 2019

“It is like you enter another planet from the atmosphere and you’re welcomed by something you never thought you’ll see at the bottom of the ocean. From the darkness of the sea, these crazy big chimneys welcome you.”
 
This is Dr. Begüm Topçuoglu (bey-goum top-cho-loh) describing her experience seeing the bottom of the bottom of the Pacific Ocean through the lenses of the remotely operated vehicle Jason II in 2015. Topçuoglu earned her doctorate studying the microbial life that exists at the bottom of the sea, giving her the opportunity to witness a possible origin of life on Earth, firsthand.
 
Figure 1. Dr. Begüm Topçuoglu piloting the Jason II ROV on the 2015 Axial Seamount Expedition. Image courtesy B. Topçuoglu.

The chimneys that Topçuoglu refers to are deep-sea hydrothermal vents. Superheated water pours from these vents after having passed by magma-heated rocks underneath the earth’s crust. Boiling out at 400°C, the vent water rapidly cools in the surrounding ocean, making the water shimmer like the heat waves that rise off hot pavement in the summer.
 
Figure 2. Shimmering water (top) is released from a deep-sea vent covered with tube worms (red) that form a symbiotic relationship with chemotrophic microbes to gain nutrients. Image courtesy B. Topçuoglu, Axial Seamount Expedition 2015.

This geothermally heated water also carries some of the most basic chemicals of life—metals and minerals like sulfur, iron, and nickel dissolved from the rock below—that have incredible potential when they interact with carbon dioxide in the surrounding ocean water. This is what led to the hypothesis that hydrothermal vents are an origin for life on Earth1.

Wait a Minute. What is That?”: Discovering Life in the Depths 

In 1973 and 1974, a group of US and French researchers undertook Project FAMOUS (French-American Mid-Ocean Undersea Study). Their goal was to study the Mid-Atlantic Ridge, a 40,000-mile-long undersea mountain range that geophysicists thought might be a seam between two tectonic plates. One of the US crew was Robert Ballard, a geologist and technical chief responsible for operation of the submersible robot, Alvin, and the eventual discoverer of the Titanic wreckage. The Project FAMOUS expedition established Ballard as a scientist and expert in deep-sea submersibles, so in 1977 when Oregon State University geophysicist Jack Corliss wanted to explore similar underwater ridges near the Galápagos Islands, Ballard tagged along. It was on this trip that hydrothermal vents were discovered.
 
“Wait a minute. What is that?”
 
“I think there’s shimmering water right over here to the left, coming out right off the top.”
 
This was Ballard and his colleagues examining underwater photos taken by the submersible Angus. Not only did the timing of these photos correspond to a massive temperature change on the ocean floor, but they contained evidence of life in a presumably cold and barren wasteland.
 
Figure 3. Tube worms and a swarm of Yeti crabs (Kiwa hirsuta) surrounding a deep-sea hydrothermal vent with shimmering water (blurry spots).

Ballard described this as “a phenomenon the world has still not fully digested: huge clusters of extraordinary and never-before-seen living creatures -- giant clams, mounds of mussels, tiny white crabs, and eight-foot red worms -- all thriving in crushing pressure and total darkness at the edge of volcanic vents thousands of feet beneath the surface where temperatures are hot enough to melt lead.”
 
But how is this biodiversity possible? Microbes.

Life in the Deep Sea

Unlike most microbes, those at the bottom of the sea don’t have access to either organic molecules like sugar to metabolize for energy, or sunlight to make their own by photosynthesis. Instead, these microbes (both bacteria and archaea) harvest their energy from the unique chemistry of hydrothermal vents through a process called chemosynthesis, which converts carbon dioxide (CO2) to organic molecules.
 
Chemosynthesis (aka, chemolithoautotrophy) was hypothesized in the 1880’s by Sergei Winogradsky, who discovered sulfur granules in bacteria isolated from hot sulfur springs. In 1981, Colleen M. Cavanaugh published evidence of bacteria housed within the red tube worms collected from hydrothermal vents. These bacteria also contained sulfur granules, the result of chemosynthesis from hydrogen sulfide, thus confirming Winogradsky’s 90-year-old hypothesis that there are bacteria capable of existing solely on inorganic chemicals.
 
CO2-fixation through chemosynthesis requires electrons, which can be supplied by hydrogen sulfide (H2S), ammonia (NH3), or occasionally hydrogen molecules (H2). Depending on the input, hydrogen reduction can result in either glucose (C6H12O6, see 4a) or methane (CH4, see 4b). The lack of oxygen and sunlight, mean that the organic molecules generated by chemosynthetic bacteria are the only source of food for those in the ecosystem such as the tubeworm.
 
Figure 4. Chemistry of chemosynthesis. a) conversion of hydrogen sulfide to glucose. b) conversion of hydrogen to methane. Figure courtesy A. Hagan.

In addition to the chemosynthetic bacteria that supply organic molecules to tubeworms, there are also important cooperative relationships between microbial species. In some deep-sea hydrothermal vents, the supply of H2 to generate CH4 is quite low, so scientists have been baffled by the relatively high amounts of CH4 at some of these locations. Topçuoglu’s research demonstrated that a microbial relationship allows this to happen at thermophilic temperatures (55 - 80ºC) despite the low environmental amount of H2  through a process called cooperative methanogenesis.
 
Using 16S rRNA gene surveys of vent fluid enriched for cooperative methanogenesis, Dr. Topçuoglu investigated the microbial taxa responsible and established a co-culture model to study the extreme environment in the lab. Her model used representative species of the two hyperthermophilic archaeal genera found in her surveys: the H2-producing Thermococcus paralvinellae and H2-consuming methanogen, Methanocaldococcus jannaschii. The H2-producing T. paralvinellae degrades organic compounds and transfers H2 to methane-forming M. jannaschii at thermophilic temperatures thus generating CH4 at hydrothermal vents where environmental H2 is scarce.

Metabolism First: A Hypothesis for How Life Began

Some scientists believe that the chemistry that enables life at the bottom of the ocean also enabled the origin of life on Earth. When the superheated alkaline vent water mixes with cooler and more acidic seawater, it creates a gradient similar to that in a battery. This aqueous battery has enough charge to:
  • generate ATP, the basic currency of life.
  • allow the catalytic metals in the vent water to fix CO2 into organic molecules (e.g., pyruvate and glyoxylate).      
But organic molecules alone do not a cell make.
 
This is where the physical structure of the hydrothermal vent chimneys comes into play. The chimneys are formed when volcanoes erupt underwater and the lava rapidly cools, leaving microscopic pores in the rocks. These pores contain catalytic metals, protons, and CO2 that generate organic molecules using the power provided by the vent battery. The flow of protons through the pores is theorized to be an early example of proton-motive force that allowed the pores to act as templates for future cells. The chemical interactions in these protocells spontaneously generate most of the reactions and intermediates of core biological pathways (e.g., Krebs, amino acid synthesis). Eventually, the interactions are believed to have created self-replicating molecules, and finally true cells with their own membranes.
 
While this “Metabolism first” hypothesis relies on a couple of key assumptions—the presence of nitrogen, catalytic iron, and more carbon dioxide in the early oceans—there is supporting evidence in the fossil record. Earth formed about 4.5 billion years ago and rocks recovered from the Nuvvuagittuq belt in Quebec, Canada suggest that microbial life existed at the bottom of the sea at least 3.770 billion years ago. In these rocks were fossilized hydrothermal-vent-related precipitates that contained the remains of iron-metabolizing filamentous bacteria.
 
Blue protozoal mats cover the remains of dead tube worms (green) at an inactive hydrothermal vent. Image courtesy B. Topçuoglu, Axial Seamount Expedition 2015.

Each hypothesis for the origin of life1 has its merits and detractors, but it is difficult to deny the beautiful and fascinating world hidden in the depths of the sea. To survive in such extreme conditions, the creatures surrounding these deep-sea vents feed on microbes with unique metabolisms. Metabolisms that give researchers hope for new antibiotics, and that there might be life underneath the oceans of other planets.
 
Footnote:
1. There are three primary hypotheses for the origin of life on Earth.
  • Panspermia, which posits that life was brought to Earth from elsewhere in the       universe via comet or asteroid.
  • RNA World,” which argues that genetic material emerged first, later developing into life.
  • Metabolism First,” the hypothesis that chemical gradients created self-replicating, organic molecules that eventually led to the cell and life.
 
Further Exploration:
  • Bacteria that respire electrons - It’s Electric! The Bacterial X-men Superpower
  • Video & Blog of the Axial Seamount Expedition (includes interview of Dr. Topçuoglu plus footage of the onboard lab and shimmering water) -- compiled and written by Rachel Teasdale, Professor of Geological & Environmental Sciences at California State University, Chico.
  • Short NOAA video on hydrothermal vents
  • What a hydrothermal vent sounds like.
  • Video of hydrothermal vents in the Marianas Trench

Author: Ada Hagan

Ada Hagan
Senior Contributor Dr. Ada Hagan works with the ASM Journals Chair Dr. Pat Schloss in the Department of Microbiology and Immunology at the University of Michigan. Her postdoctoral research focuses on representation and bias in scientific publishing, focusing on the field of microbiology. In addition to diversity, equity and inclusion, Ada is an advocate for science communication and research trainees. You can follow her on Twitter @adahagan.