A bacterium found in sewage sludge uses its tail-like flagellum to lasso a symbiotic archaeon and keep it close at bay so that the two microbial partners can synchronize their metabolism, a Japanese research team reports in the Mar. 20 issue of Science.

Scanning electron micrograph of Pelotomaculum thermopropionicum Image: PNNL

The paper is "important for understanding how organisms that are so incredibly different, at least phylogenetically, are able to cooperate," Joseph Grzymski, a microbiologist at the Desert Research Institute in Reno, Nevada, who was not involved in the study, told The Scientist.

Pelotomaculum thermopropionicum, a fermenting, anaerobic bacterium found in wastewater treatment reactors, and Methanothermobacter thermautotrophicus, a helper archaeon that takes the bacterium's hydrogen byproducts and turns them into methane, form a type of mutually-beneficial relationship based on nutrition known as syntrophy. This prokaryotic partnership was known to be mediated through some sort of stringy filaments, but it wasn't clear what physical processes or chemical communiqués made the alliance achievable.

Kazuya Watanabe and his colleagues at the University of Tokyo analyzed the genomes and cellular dynamics of the two microbes, and showed that when the archaeon bound a particular protein in the bacterium's flagellum -- the flagellar filament capping protein FliD -- many of the archaeon's genes became activated, including those involved in methane production.

Unlike other microbial communications systems such as quorum sensing, which rely on small molecules, "this is the first discovery for protein-mediated communication between prokaryotes" of different species, said Watanabe in an email. "Yet, I think similar mechanisms are widespread in the prokaryote world."

The bug bond could help explain the origin of the eukaryotic cell, noted Michael McInerney, a microbial physiologist at the University of Oklahoma in Norman who did not contribute to the research findings. The "hydrogen hypothesis" -- first proposed in 1998 by the University of Düsseldorf's William Martin and Rockefeller University's Miklós Müller -- postulates that a symbiosis between bacteria and archaea based on hydrogen metabolism led to the first complex eukaryotic structures, such as mitochondria. The flagellum-based association "could be somewhat of a remnant of that," said McInerney. "Through geological time, there could have been a variety of associations."

The "primordial communication scenario" also offers clues about more complex inter-species interactions, such as those between mammalian immune systems and pathogenic bacteria, said Grzymski. Toll-like receptors in the innate immune system are known to detect flagellar proteins to initiate immunity-related signaling cascades, he noted. So, this paper "will give people more insight into how higher organisms are able to detect and send off pathogens."

Klaus Winzer, a molecular microbiologist at Nottingham University, UK, called the paper "fascinating," but he noted that "further mechanistic insights are required before final conclusions [about the nature of the interaction] can be drawn." Grzymski agreed. "What they don't show is whether or not this is occurring all of the time," he said. "What is the on-off mechanism? Is it distance? Is it concentration?" Watanabe said that his team is currently working to sleuth out the details of the signal transduction system.


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Flagellar tangle
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