Yucatán’s Underwater Caves Conceal a Diversity of Microbial Life

With the help of an experienced underwater cave diving team, Northwestern University researchers have created the most complete map yet of the microbial communities living in the submerged labyrinths beneath Mexico’s Yucatán Peninsula.

While previous researchers have collected water and microbial samples from cave entrances and easily accessible sinkholes, the Northwestern-led team reached the deep, dark passages of unlit waters to better understand what can survive in this unique subterranean realm .

After analyzing the samples, the researchers discovered a system rich in diversity, organized in different patterns. Much like a stereotypical high school lunchroom, microbial communities within the cave system tend to cluster into well-defined cliques. But one bacterial family (Comamonadaceae) acted as a popular social butterfly, appearing at almost two-thirds of the ‘cafeteria tables’. The findings indicate that Comamonadaceae are the ecological hub of the broader community.

“This is certainly the most comprehensive microbial study in this part of the world,” said Magdalena R. Osburn of Northwestern, who led the study. “These are incredibly special samples from underground rivers that are extremely difficult to obtain. From those samples we were able to sequence the genes of microbial populations living in these locations. This underground river system provides millions of people with drinking water. So whatever happens to the microbial communities there has the potential to be felt by people.”

Osburn, a geobiology expert, is an associate professor of earth and planetary sciences at Northwestern’s Weinberg College of Arts and Sciences. Northwestern alumnus Matthew Selensky led this project as part of his dissertation when he was a graduate student in Osburn’s lab. Study co-author Patricia Beddows, a Weinberg professor of earth and planetary sciences, led the cave diving expedition, drawing on her decades of experience working on these caves. Other Northwestern co-authors include Andrew Jacobson, professor of earth and planetary sciences, and former graduate student Karyn DeFranco, who focused on geochemistry.

Located mainly in southeastern Mexico, the vast Yucatán carbonate aquifer is pockmarked by numerous sinkholes that lead to a complex web of underwater caves. The underwater network harbors a diverse but understudied microbiome and includes areas of freshwater, seawater, and mixtures of both. The system also includes a variety of zones: from pitch-black, deep pits with no direct openings to the surface to shallower sinkholes that glisten with sunlight.

“The Yucatan Platform is essentially a Swiss cheese of cave channels,” Osburn said. “We were curious about which microbes are found together when we look at the entire system versus which microbes occur within one ‘neighborhood’.”

To investigate this question, a team of cave divers collected 78 water samples from 12 individual sites within the cave system near the Caribbean coast in Quintana Roo, Mexico. The sample collection extended from the Xunaan Ha system at the northern end to inland and coastal portions of the Sac Actun system (including a prominent, 60-meter deep pit) to the Ox Bel Ha system at the south.

Back at a dive shop turned science laboratory, researchers filtered cells from each sample and analyzed its chemistry. Then, back at Northwestern, they identified microbial communities by sequencing their DNA. Selensky then developed a new computer program to perform network analyzes on the data set. The resulting networks showed which species tend to live together. For each site, the researchers took into account the environmental context of each microbial community, including cave type (pit or pipe), cave system, distance from the Caribbean coast, geochemistry and position in the water column.

Although water from the Gulf of Mexico flows into the Yucatán aquifer, the aquifer’s microbiome varies significantly from the nearby sea, the researchers found. The microbiomes also vary throughout the cave system: from cave to cave and from shallow water to deep water.

“The microbial communities form different niches,” Osburn said. “There is a changing cast of characters who seem to move depending on where you look. But if you look at the entire data set, you see a core group of organisms that seem to play a key role in every ecosystem.”

Osburn and her team discovered that Comamonadaceae, a bacterial family commonly found in groundwater systems, lived in different niches. They also found that a deep, pit-like sinkhole with an opening at the surface (which allowed sunlight to enter) housed the most microbial communities – separated into layers of different niches in the water column.

“It appears that Comamonadaceae plays slightly different roles in different parts of the aquifer, but it always plays an important role,” Osburn said. “Depending on the region, it has a different partner. Comamonadaceae and its partners probably have a mutualistic metabolism, perhaps sharing food.”

Reference: Osburn MR, Selensky MJ, Beddows PA, Jacobson A, DeFranco K, Merediz-Alonso G. Microbial biogeography of the eastern Yucatán carbonate aquifer. Speer JR, ed. Appl Environmental Microbiol. 2023: e01682-23. doi: 10.1128/aem.01682-23

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