Unicellular Predators Feast at Hydrothermal Vents

Citation: Hu, S. K., Herrera, E. L., Smith, A. R., Pachiadaki, M. G., Edgcomb, V. P., Sylva, S. P., Chan, E. W., Seewald, J. S., German, C. R., & Huber, J. A. (2021). Protistan grazing impacts microbial communities and carbon cycling at deep-sea hydrothermal vents. Proceedings of the National Academy of Sciences, 118(29).

Hydrothermal vents are oases of life in the deep sea, and their inhabitants – tube worms, “eyeless” shrimp, single-celled microbes, and other creatures – have captured the imaginations of many. While life at the ocean surface depends on sunlight, organisms at hydrothermal vents have adapted to life in the dark, and instead depend on the chemicals contained in vent fluids to generate energy. This unusual way of life is known as chemotrophy.

But where do these life-sustaining hydrothermal fluids come from?

Hydrothermal vents typically form along tectonic plate boundaries – specifically at “divergent boundaries” where the plates are moving away from one another. Hot magma from the Earth’s interior rises to occupy the newly created space between plates, and cools when it contacts cold seawater circulating in porous sediments. The seawater heats up, collects mineral particles from the magma, and then escapes upward into the water column, pulling more seawater from neighboring sediments to take its place. The continuous flow of heated, mineral-rich fluid at the plate boundary creates a long-lasting hydrothermal vent habitat (Figure 1).

Figure 1: A schematic of a hydrothermal vent, depicting the circulation of seawater through sediments and its ultimate emission from the seafloor. (Image Source: NOAA)

Oases of Life

Chemotrophs (the microscopic organisms that generate energy from chemicals) represent the base of the hydrothermal vent food chain. These chemotrophs are members of the domains Bacteria and Archaea – two of the three main branches on the tree of life (Figure 2). They convert methane, hydrogen sulfide, metals, and other vent fluid components into their body mass, and are intensively studied by marine biologists due to their unique metabolisms and abilities. The organisms at the top of the food chain – such as tube worms, shrimp, and eels – are also well studied. These organisms are typically large, multicellular Eukaryotes (the third domain of life), and studying them has helped unlock the secrets of convergent evolution and symbiosis, among other topics. However, very little is known about the missing link in the hydrothermal vent food chain: protists.

Figure 2: The tree of life, which separates the three major domains: Bacteria, Archaea, and Eukarya. Protists are a diverse group of organisms and are highlighted in yellow. (Image modified from Wikimedia Commons)

Protists are single-celled organisms at a very interesting location on the tree of life. They belong to the same domain as humans – Eukarya – and are more closely related to humans genetically than they are to Bacteria and Archaea. However, they’re an extremely diverse group of organisms, and their role in deep-ocean food webs is particularly nebulous. A team of scientists from the Woods Hole Oceanographic Institution (WHOI) decided to investigate that role. Do protists – which eat chemotrophs and subsequently get eaten by larger Eukaryotes – make a substantial dent in the chemotrophic population?

Predation by Protists

Figure 3: The location of the Gorda Ridge in the northeastern Pacific Ocean. (Image Source: Wikimedia Commons)

To collect protists for their experiments, the team traveled to the Gorda Ridge (Figure 3) – a tectonic plate boundary in the northeast Pacific Ocean (roughly 100 miles off the coast of Oregon). At the ridge, the Pacific plate is slowly separating from the Gorda plate, and hydrothermal vents are abundant. Using a remotely operated vehicle (ROV), the team sampled fluids from several different vents, as well as from a non-vent site nearby. They brought the fluids back to the lab in separate bottles and set up a series of experiments.

First, large multicellular organisms (large Eukaryotes) were filtered out of the bottles of seawater, leaving only protists and their chemotrophic prey. Then, special fluorescently labeled prey was added to the seawater, which had been modified to glow under a microscope. Over several days, the researchers analyzed the density of glowing prey in the bottles of hydrothermal fluid to determine how quickly the protists were grazing on chemotrophs.

As expected, prey density decreased over time as the protists consumed their food. However, the researchers observed that predation was much faster in the bottles with hydrothermal vent fluid, rather than the non-vent fluid. In fact, protists at vents consumed between 28 and 62% of the entire prey population every day, meaning that protistan predation drives extremely high turnover of chemotrophs. The prey preferences of protists also help select which chemotrophs populate vents.

Implications for the Carbon Cycle

This research provides the first-ever estimates of protistan grazing pressure at hydrothermal vents and suggests that protists have an important role in the carbon cycle there. Because protists transfer so much organic matter up the food chain at vents, and exert so much pressure on the chemotrophic population, the researchers suggest that efforts to characterize the amount of recycled carbon should include protists in calculations. The researchers also caution that before deep sea locations are disturbed for mining operations (for extraction of fuel or valuable metals), it’s vitally important that we understand the biological processes that are currently operating, and the food webs we might unknowingly disturb.

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