No microbiome is an island, unprecedented survey of Hawaiian valley reveals

LOUISVILLE, KENTUCKY—Even the internal world of microbes on which almost every plant and animal depends is part of a larger ecosystem, findings from a Hawaiian valley suggest. Researchers have tended to study such microbial communities—found in animal guts and in nitrogen-fixing nodules on legume roots, for example—in isolation. But by sampling and analyzing bacteria throughout Oahu’s Waimea Valley, a team has found that each organism’s microbiome is a subset of what exists in the broader environment and in organisms lower on the food web. “The real surprise was the extent to which microbes are spread across hosts and habitats,” said microbial ecologist Anthony Amend, one of about two dozen researchers at the University of Hawaii (UH) in Honolulu who conducted the survey. “We have been wearing blinders.”

Instead of individual microbiomes, picture a single “ecosystem microbiome,” says Amend, who presented the findings here at the annual meeting of the Ecological Society of America this month. The work “has the possibility of giving us a whole picture of how microbes move within and across environments,” adds Kabir Gabriel Peay, an ecologist at Stanford University in Palo Alto, California, who heard the meeting presentation. “This approach is really critical if we really want to know how microbiomes assemble.”

UH’s Margaret McFall Ngai, whose studies of bioluminescent microbes in squid over the past several decades revealed how intimate the connections between microbes and their hosts can be, thought the Hawaiian islands might do for microbes what they have for other flora and fauna: provide a laboratory for testing key ecological principles. And she realized that newly hired UH microbiome researchers had the range of expertise needed to do the work. Her colleagues were quickly sold on the idea, and they identified the Waimea Valley as a promising setting. A watershed just 12 kilometers long, Waimea encompasses a wide range of habitats, from dry beach to tropical rainforest.

Students and faculty fanned out across the valley to collect microbes, sampling plants, animals, soil, rocks, streams, and even the ocean, as divers took stock of the microbes in the coral reefs at the valley’s base. They analyzed all the DNA in their samples and compared those sequences to DNA databases of known organisms. “I can’t think of anyone else who has taken that [broad brush] effort,” says Stephanie Kivlin, a microbial and ecosystems ecologist at the University of Tennessee in Knoxville. “We never thought to look how [the microbes in] nearby animals might affect the plants,” she adds. “What they found is that there’s this really nice pattern.”

The data revealed nested microbiomes, akin to Russian dolls. The soil and free-living samples contained the widest range of microbes. Primary producers—plants and algae—hosted the next greatest range, although just a subset of the diversity seen in the valley environment. The plant and algae eaters had a subset of that subset, and carnivores had the least diverse microbiomes of all. Amend and his colleagues concluded that the microbes in the landscape set the stage for those found within hosts. And somehow each organism’s place in the food web helps determine what microbes it acquires.

Many researchers have assumed that an organism’s microbiome is somehow seeded from the environment, but few had delved into the specifics. This study is “a demonstration of how connected our world is, all the way down to the microbiological level,” says Colin Averill, a microbial ecologist at ETH Zurich in Switzerland who studies how soil microbes influence the trees above them. The Waimea survey “implies that I need to take an even broader approach,” he says.

The work also revealed that some microbes are surprisingly widespread. Many so-called marine fungi were common in the stream and even on land, Amend reported. That’s surprising to Peay. “It suggests that they may have much more complex life cycles or natural histories than we have previously imagined.”

Amend and his colleagues now hope to watch the ecosystemwide microbial traffic in action. They are taking lab-grown strawberry seedlings and caged, lab-reared, germ-free fruit flies to different places in the valley, hoping to see how they acquire microbiomes from the environment and how their new microbial guests affect their health and reproductive fitness. “That could have a practical payoff,” Peay says. “Understanding how plants and animals acquire their microbiomes has the potential to improve efforts to restore ecosystems, improve agricultural sustainability, and manage diseases.”