by Janie
In storytelling, there is a famous principle called Chekhov's gun. "If in the first act you have hung a pistol on the wall, then in the following one it should be fired. Otherwise, don't put it there." This pithy (and very debatable) directive, attributed to the eponymous playwright, smells a whole lot like the (similarly very debatable) viewpoint of adaptationism in evolutionary biology, if the firearm here were some organismal trait and the firer were evolution.
Regardless of its usefulness or un-usefulness, it's at the very least a little nudge to drive some musing about the why and what of some unexpected bit of biology – all the woulda coulda shoulda's of an evolutionary story.
Fig. 1. Migration of V. fischeri to nucleosides and their components. V. fischeri cells were inoculated onto Tris-buffered TB-SW soft agar plates for 5 h at 28°C. A. Thymidine (T) and serine (S) were spotted just beyond the migrating rings of V. fischeri. B. Serine (S) and cytidine (C) were spotted just beyond the migrating rings. C. Uridine (U), uracil (u), ribose (R), and deoxyribose (dR) were spotted onto plates just beyond the migrating rings. An excess of serine (S) was spotted at the top of each plate as a comparison. Source. Frontispiece: Hawaiian bobtail squid (Euprymna scolopes). Source
So, here is an interesting scenario fished out from the light organ symbiosis between the bobtail squid and the bioluminescent Vibrio fischeri, an intricately choreographed mutualism. A paper from 2003 reported that symbiotic V. fischeri migrates towards and consumes all four ribonucleosides and all four deoxyribonucleotides. There hasn't been a follow-up on this since then, and so the question still burns: why would V. fischeri exhibit chemotaxis towards nucleosides and nucleotides?
Chemotaxis towards nucleosides/tides is unusual but not unheard of. In the vertebrate immune landscape, for one, nucleotides appear to be key signaling molecules amongst macrophages, the cellular clean-up crew that deals with detritus and dead cells among many chores. This makes sense. A damaged cell will leak its contents, so freely flowing extracellular ATP is a smoking gun. Cells undergoing apoptosis, too, send out ATP and UTP like molecular flare signals, which guide patrolling macrophages to the site to come clear away their remains. Some macrophages release nucleotides themselves; in this case the respondents appear to be neutrophils.
In some bacterial lifestyles, too, it's handy to be able to sniff out extracellular nucleotides or parts thereof (e.g., nucleobases). For a saprophyte, for instance, following that scent trail to come upon a dead cell equates to a nice meal. This seems to be the case for Pseudomonas putida, which is attracted to pyrimidines, cytosine in particular, via the chemotaxis protein McpC (a finding reported in 2009), and to purines via the chemotaxis protein McpH (a finding reported in 2016). For a pathogen, too, extracellular nucleotides or their components could handily signal a damaged cell. Campylobacter jejuni, for example, is attracted to purines (a finding reported in 2021; pyrimidines were not tested). The only other reported examples of this kind of chemotaxis appears to be the case of E. coli RP437, which is attracted to pyrimidines (a finding reported in 2008; purines were not tested). Different bacteria appear to have preferences, since for E. coli, cytosine has barely any effect while thymine and uracil are potent chemoattractants, in contrast with P. putida with its affinity for cytosine. Nucleobases seem to be acting as the saprophyte's equivalent of blood in the water to a shark.
With this hypothesis in mind, the case of the symbiotic strain of V. fischeri appears odd: here it is in a mutually "happy" relationship in which both organisms are alive and well, unlike the pathogen or saprophyte example, and yet it so drawn to every nucleoside/tide. Other chemoattractants for V. fischeri, meanwhile, are less surprising: amino acids including serine; N-acetylneuraminic acid, a sugar found in the mucus surrounding the squid light organ; and two sugars found inside the light organ, chitobiose and N-acetylglucosamine (GlcNAC), the breakdown products of squid-produced chitin. Nothing out of the norm here – lots of bacteria are lured to the siren song of amino acids and sugars. The Vibrio symbionts, tasked with the extremely bioenergetically costly responsibility of bioluminescence, certainly wouldn't turn down an offering of convenient energy sources.
Fig. 2. Migration of V. fischeri to nucleosides and their components. V. fischeri cells were inoculated onto Tris-buffered TB-SW soft agar plates for 5 h at 28°C. A. (From Fig. 2 from source paper) Enumeration of hemocytes present during the day (10 hours post-dawn; white box) and night (22 hours post-dawn; black box) in light-organ tissues of two-day-old immature symbiotic (solid bars) or aposymbiotic (hatched bars) squids. B. (From Fig. 1 from source paper) Confocal micrograph showing colocalization of chitin (green) and hemocytes (red) in central-core tissue of the squid light organ (blue). Tissue was sampled just before nightfall (10 hours post-dawn). Source.
Why, then, might V. fischeri be drawn towards dead and dying cells? This moribund attraction seems to make more sense in light of the biological interplay of the mutualism. Throughout the 24 hours of the day, the squid host traffics hemocytes (the invertebrate equivalent of macrophages) in and around the cavern-like crypts of the light organ where the spelunking symbionts reside. These hemocytes help prevent other bacterial species from getting in. But when the sun goes down – when the symbionts must get down to business and glow – the squid sends extra hemocytes, which undergo lysis and provision the hungry symbionts with their own chitin.
But wait, red herring – this carrion-scavenging is not unique to V. fischeri and its symbiotic role. Free-living V. fischeri and plenty of other species in its genus are saprophytic feeders in the marine environment. As it turns out, it was already postulated in the 90's that Vibrios as a whole genus are attracted to the released contents of injured marine organisms, a piñata panoply of sugars like glucose and trehalose – and nucleosides/tides. It is untested whether migration towards nucleosides/tides is a unique trait or one that is shared by other Vibrios, or also whether there is a difference in this behavior between symbiotic and non-symbiotic strains of V. fischeri.
The chemotaxis of V. fischeri towards nucleosides/tides does not seem to be driven by the purpose of snatching up the ribose as a carbon source, since the bacteria do not migrate towards the isolated sugar. It is possible that the nucleobases serve as a handy nitrogen source, but the ability to do this bit of metabolism is not uncommon amongst bacteria. Comparative studies with its less pleasant relative, V. cholerae, would be interesting. In V. cholerae, nucleoside transporters seem only to confer a fitness advantage when transitioning from a living host to an aquatic environment; the suggestion is that nucleoside uptake only becomes important when the bacteria transition from a nutrient-rich environment to a nutrient-poor one. Whether this translates over into V. fischeri is not known. The other intriguing tidbit is that free cytidine is a repressor of natural competence in V. cholerae.
(The other interesting chemoattractant that appears to be unique to V. fischeri amongst other Vibrios is N-acetylneuraminic acid, a sialic acid found in the mucus used by baby squids to snag their first symbionts out of surrounding seawater. Only symbiotic V. fischeri respond to it while the other tested Vibrios, V. anguillarum and V. parahemolyticus, do not. It's possible the symbionts use this nine-carbon keto acid as a gourmet carbon source, not unreasonable to guess since human pathogens lurking around mucus membranes do, too. Another idea is that the symbionts – as symbionts are wont to do – have taken a page even more directly out of the pathogens' book: sprucing themselves up with this cell surface indicator of healthy eukaryotic mucus membranes, in order to avoid being sniffed out by the immune system.)
Whatever the case, V. fischeri doesn't skimp on chemoreceptors; it has 43 of them encoded in its genome (compare this to the number of E. coli chemoreceptors, which can be counted on one's own hands). There have been attempts to pinpoint the specific receptors of chemoattractants by knockout mutations, as has been accomplished in other bacteria, but efforts have been slow-going. The genetic framework underlying the bacterium's chemotaxis behavior is not that simple, and the mishmash of interwoven receptor pathways is difficult to disentangle.
(Also: Chekhov's gun, mentioned at the beginning, does not really have very much to do with this little romp through the literature. That mention was just to poke fun at it, because having brought it up again just now in closing makes this all a meta-Chekhov's gun.)
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