by Roberto
When I started graduate school at UCSD in the mid-1970s, I sometimes found myself hitchhiking at dawn along the Pacific Coast from Solana Beach to the lab. There were some wild rides! Which is probably why some years later, as they crossed my path, I was attracted both to "The Hitchhiker's Guide to the Galaxy" and (in biology) to the evolutionary and ecological concepts of hitchhiking. In evolution, it refers to neutral alleles that are inherited because they are closely linked to alleles under selection. In ecology, sometimes called phoresis, it is the attachment of an organism to another for the purposes of travel. This is a very common and widespread strategy for organisms to improve their dispersal, usually in search of "greener pastures." In an earlier post I presented the example of a hitchhiker moth that travels by residing in the green sloth, thus gaining easy access to the sloth's droppings, where it must deposit its eggs. Importantly and more germane to STC, as most of our readers will know, hitchhiking abounds in the microbial world.
Fig. 1. An Illustrated Overview of Microbial Hitchhiking Reports. Source
For many years now, at STC we've been fascinated by the wild rides of microbial hitchhikers. We described how Streptomyces spores hitch a ride by sticking to Bacillus subtilis flagella for local journeys or by emitting geosmin to attract springtails they are transported to faraway lands. And long before, there was Elio's 2012 post on how Paenibacillus transports fungal spores and even latex beads. Covering the subject much more comprehensively, there is an outstanding review by Alise Muok and Ariane Briegel. With this beautiful set of drawings (Fig. 1), they nicely summarize the reports of intermicrobial hitchhiking. The legend to the figure describes the stories: "(A) Paenibacillus vortex and Acinetobacter baylyi (orange cells) can push immotile bacteria at the colony's leading edge (blue cells). P. vortex can push antibiotic-resistant cells (blue cells) at the colony's front, and these cells hydrolyze antibiotics (red background) to nonlethal substances (white background). (B) P. vortex (orange cells) can serve as a raft for the phytopathogen Xanthomonas perforans(red cells) for transport across plant leaves. (C) Staphylococci (pink cells) can attach to the cell body of motile bacteria (teal cells) and form communal biofilms with the motile partners. (D) Capnocytophaga gingivalis (gray cells) can transport various immotile microbes (multicolored cells) to establish communal biofilms with specific spatial features (right). (E) The immotile spores of the bacterium Streptomyces and the fungus Aspergillus(brown cell) are transported by swarming bacteria (blue cell) via direct attachment to flagella. (F) Legionella pneumophila (red cells) are aquatic bacteria that are free-living or infect amoebae (white cell). (G) Immotile Deltaproteobacteria (yellow cells) that possess ferromagnetic particles (black dots) can adhere to the surface of some protists (green organism) to create a microbial consortium that is capable of magnetotaxis." Their enthusiasm for this topic is clear: "We predict that intermicrobial hitchhiking will develop into an independent subfield in microbiology..." I very much agree that this subject should receive much more attention as investigators delve deeper into natural settings and study not only community composition but also the dynamics of microbial migrations within those communities.
Not unexpectedly, now there are reports of phages as hitchhikers. I came across two thought-provoking papers recently. In both, the authors use greatly simplified (thus highly controllable) microcosm setups to test some basic ecological concepts. While these do not faithfully reproduce natural settings, the results provided me with much food for thought.
Fig. 2. By mixing the E. coli phage PHH01 with motile B. cereus in a flow cell, phage reached and infected the E. coli in the submerged biofilm more effectively that in the absence of B. cereus. In addition, when mixed with the phage, B. cereus colonized the preformed E. coli biofilm more effectively than in the absence of phage. Adapted from source.
One paper, by Yu et al., describes a flow-cell system with a chamber containing a submerged, preformed Escherichia coli biofilm. High over the biofilm they flow a solution that can contain either Bacillus cereus, the coliphage PHH01, or a mixture of both. The B. cereus alone reaches the biofilm and colonizes it albeit not very effectively. And, at high flow rates, when alone the phages do not reach the biofilm – they are washed out through the outlet of the chamber. But when phage and B. cereus are mixed before entering the chamber, both reach the biofilm. They go on to show microscopically that the phages attach to the B. cereus flagella. Clearly, the phages are hitching a ride on the bacteria. Interestingly, a consequence of B. cereus cells arriving loaded with phages on their flagella is that some of the E. coli get infected and lyse, leading to a much-increased colonization of the preformed biofilm by the invading B. cereus. The authors did one more experiment as a first step to see if this could be a general process with other phages. They took wastewater effluents and using metagenomic sequencing determined the composition of its phage community. They then mixed the effluent with B. cereus flagella and sequenced the bacteriophage community that attached. In short, members of at least ten phage families stuck to the flagella. So yes, this hitching a ride on flagella may well be a widespread phenomenon.
Fig. 3. Top: scheme of the microcosm setup specifying microbial inoculation points. Bottom: Helium ion microscopy (HIM) visualization of T4 phage adsorption to E. coli host and non-host P. putida KT2440 cells (a) tail-mediated adsorption to E. coli host cells and (b) capsid-driven adsorption to non-host P. putida KT2440. Adapted from source.
That's all fine and well for aquatic systems, but what might happen in soils? The authors of the second paper, by You et al., addressed the question of whether phages could hitchhike in such "water-unsaturated" settings, with dry grains and air-filled spaces. They relied on the concept of "fungal highways," where wet fungal hyphae serve as waterways that allow motile bacteria to swim along dry soil grains and even across air holes. Their model microcosm had two blocks of agar, separated by an air gap (Fig. 3, top). On the left side they inoculated the filamentous fungus Pythium ultimum. As the fungus grew, its hyphae could span the air gap and continue growing on the right side. They then inoculated Pseudomonas putida on top of the fungus on the left side and E. coli on the right to pre-colonize that agar surface. Finally, they added coliphage T4 to the right side. (Of course, they carried out all the appropriate controls: for example, no fungus, no phage, no P. putida, no E. coli, and importantly, non-motile P. putida.) Interestingly, when they examined the phage attachment to P. putida, they were not attached to the flagella. Rather, they were lying down flat on the surface of the cell (Fig. 3, bottom). Not that it matters, just goes to show that when it comes to hitchhiking, phages seem to grab whatever surface they can. But by lying flat, they kept their tail fibers at the ready in case they happen to run into a susceptible E. coli. And that's what seems to happen.
Fig. 4. The main findings of the study are summarized and illustrated. Boxes and contents are directly mirrored from the recently published MAcroecological Framework of Invasive Aliens (MAFIA). Adapted from source.
The main findings of this second study are summarized in Fig. 4. T4 can hitch a ride on P. putida which, using flagella, can move along P. ultimum hyphae (the so-called "hyphosphere"). The benefits to T4 and P. putida are apparent when they reach the space pre-colonized by E. coli. T4 infect some of the E. coli and increase in number. The demise of some of the E. coli in turn gives P. putida a great increase in fitness (denoted by W in the figure). The authors make a point that their findings have many of the features that theoretical macroecologists posit as "rules" of invasion ecology, particularly as it relates to the ideas proposed recently under the named "MAcroecological Framework of Invasive Aliens" (MAFIA). Given that invasion ecology with plants and animals is not easily addressed in a controlled way, they put forth their system as a good model for such studies. Sounds good to me, always excited by any easily controlled system where general ecological principles can be put to the test. But what makes me most excited about this system is the potential for future experiments in quantifying evolutionary processes. When I see these phages hitchhiking, I envision many of them as transducing particles, carrying not phage genomes but chromosomal fragments of their prior host. These encapsidated chromosomal fragments can now travel long distances and eventually find an appropriate host living in a different ecological niche which can benefit from gaining some new genes, horizontally. These systems seem nicely suited to study the details of "the evolutionary play acted out in the ecological theater." Hope someone out there who is still at the bench thinks likewise.
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