Organ structure and bacterial microbiogeography in a reproductive organ of the Hawaiian bobtail squid reveal dimensions of a defensive symbiosis
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Abstract
Many plants and animals house symbiotic microorganisms in specialized tissues or organs. Here, we used multidimensional in-situ imaging techniques to illuminate how host organ structure and bacterial microbiogeography contribute to the symbiotic function of an organ in the Hawaiian bobtail squid, Euprymna scolopes . Along with the well-studied light organ, female E. scolopes harbor a community of bacteria in the accessory nidamental gland (ANG). The ANG is a dense network of epithelium-lined tubules, some of which are dominated by a single bacterial taxon. These bacteria are deposited into squid eggs, where they defend the developing embryos from harmful biofouling. This study used a combination of imaging techniques to visualize different dimensions of the ANG and its bacterial communities. Imaging entire organs with light sheet microscopy revealed that the ANG is a composite tissue of individual, non-intersecting tubules that each harbor their own bacterial population. The organ is bisected, with tubules converging towards two points in the organ. At these points, tubules empty in a space where bacteria can mix with squid jelly to be deposited onto eggs. Observations of bacterial populations correlated bacterial taxa with cell morphology and show that tubule populations varied: some contained populations of mixed phyla while some tubules contained only one genus of bacteria. Together, these data shed light on how bacterial populations interact within the ANG and how the host uses physical structure to maintain and employ a symbiotic bacterial population in a defensive context.
IMPORTANCE
Sequence-based microbiome studies have revealed much about how hosts interact with communities of symbiotic microbiota, but often lack a spatial understanding of how microbes relate with each other and the host in which they reside. This study used a combination of microscopy techniques to reveal how the structure of a symbiotic organ in the female bobtail squid, Euprymna scolopes houses diverse, beneficial bacterial populations and deploys them for egg defense. These findings suggest that spatial partitioning may be key to harboring a diverse population of antimicrobial-producing bacteria and establish a foundation for further understanding how host structures mediate symbiotic interactions.
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To clarify, every ANG organs were occupied by symbionts, but roughly 65% of the many tubules in each ANG contained symbionts. It may be that the "empty" tubules are the part most distal from the end where they empty into the intergland space, similar to how a tube of toothpaste is emptied. I would doubt that it light triggers the peristaltic motion since the squid starts laying eggs often later in the night and she must cover many eggs with the bacteria. Muscles cells appear to line tubules, so it appears to likely be driven by those.
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It may be different for different taxa. Many of the Alphaproteobacteria were in mixed tubules. However, sequence analysis has shown that there is greater diversity within the Alpha clade. The Verruco appear to have fewer representatives present in the ANG, and I'd imagine that because of this, there would be fewer chances for there to be tubules with mixed populations of Verruco
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That's a good point! Microvilli and cilia have been seen on many, but not all tubules of the ANG. However, we didn't correlate these with the bacterial taxon present in the tubule and didn't want to imply they were present with those specific bacterial taxa. It'll be good to add those to these to some tubules though.
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The taxonomic-specific probes were all applied to the same section, and the eubacterial probes were applied to the section immediately serial to the taxa-specific section
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These mixed tubules may result from direct interaction between community members, e.g. Alphaproteobacteria invading tubules of other bacteria, perhaps by migrating through the interstitial region between tubules or from the intergland space. This spatial localization has physiological implications: the high density at which Alphaproteobacteria bacteria inhabit tubules, along with their ability to cohabit with or invade tubules of different bacteria, likely accounts for the group’s predominance in the adult ANG bacterial community.
Is it possible to disturb the ANG microbial community by using antibiotics? If so, it would be interesting to look at how th populations rebound during the recovery phase.
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Although tubules containing mixed populations were infrequent, they were observed in every biological replicate (n=5).
Do you suspect that populations within more tubules are mixed if you were able to resolve lower levels of phylogenetic classifications?
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A peristaltic motion appears to push the tubule’s contents into the intergland space (Supplemental Video 4), and the cilia lining the NG and ANG in the intergland space may facilitate the mixing of bacteria and jelly as well as the transport to the egg.
This observation is intriguing. Do you think that this is a rare occurrence, given how only 50-75% of the ANGs were occupied by symbionts? Any ideas what might trigger the peristaltic motion and whether it could be triggered by environmental light, like the light organ venting process?
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Figure 7
This model sheds new light on the biophysical processes involved in ANG microbiogeography. I noticed that protrusions are lacking from the epithelial cells lining the tubules deep in the ANG (Fig 7B). Do you have any insight into whether these epithelia are microvillous like the light organ crypts or ciliated like the preceeding portions of the ANG and intergland space?
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These slides only had FISH probes targeting Alphaproteobacteria, Gammaproteobacteria, and Verrucomicrobia, hybridized as described above.
Were these slides sequential slices from the same ANG or were they ANGs from the five different animals?
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