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Intergenerational microbial transmission in the little skate (Leucoraja erinacea)

Katelyn Mika, Alexander S. Okamoto, Neil H. Shubin, David B. Mark Welch

Preprint posted on December 30, 2020 https://www.biorxiv.org/content/10.1101/2020.12.30.424594v1.full

Updated prelight post about the bacterial communities of sea dwellers - little skates. Now with the response from authors Katelyn Mika and Alexander Okamoto!

Selected by Kiran Gurung

Categories: ecology, genomics, microbiology

 

little skate

Figure: Little skate. Image source: Andy Martinez, NOAA 

 

Background

Elasmobranchs (which include sharks, rays and skates) are groups of fishes that have cartilaginous bones. These organisms have 5-7 pairs of external gill clefts and their skin is made up of placoid scales or dermal denticles. Some of them reproduce by laying eggs (oviparous reproduction) while others give birth to their young ones (viviparous mode).

 

Some of the key research areas related to these organisms revolve around studying their diversity, their families, ecology and their conservation status. Another key factor is understanding the microbial community dynamics and transmission patterns in these organisms. A handful of studies have profiled the microbes from guts or skins in a few species such as sharks, skates or ray fishes. In addition, a few studies in elasmobranchs have also reported about both environmental (i.e. horizontal) as well as vertical (i.e. parental) transmission. However, these studies have focussed on adults, leaving a lot to explore by investigating the microbiomes in these organisms during their early developmental stages such as juveniles.

 

In this study, the researchers profiled the bacterial communities of the egg-laying little skates, which are found in the North Atlantic Oceans. They have attempted to trace the transmission pattern of the bacterial members by sampling their diversity at six time-points during their development.   In the egg, embryonic development occurs in 33 stages and lasts 6-12 months depending on environmental conditions. When embryonic development is still in progress, at some point the egg capsule partially opens, allowing contact with the surrounding sea water. Researchers used the 16S rRNA gene sequencing method to look into the bacterial communities of the skate Leocoraja erinacea. For bacterial community profiling, they sampled external and internal gills, embryonic skin as well as adult skin.

 

Key points in this paper

 

  • Higher taxonomic richness was observed in the egg capsules and the internal liquid fluid just lining the inner shell. This changes at stage 16 (one of the earliest stages when the embryo can be visually determined), when the abundance of two Actinobacteria and Bacilli decreases, with a corresponding increase in Bacteroidetes and Planctomycetacia.

 

  • During the early stages, bacterial microbiomes of gill and embryonic skin appear similar. But this changes during the adult stage, when the gill constitutes a distinct microbiome, with Nitrosopumilus, being the core bacteria. This bacterium is associated with urea metabolism, a main metabolic activity for the gills.

 

  • Additionally, the functional predictions of the sequences in gill samples identify several molecular transport pathways which are involved in the gas exchange that takes place in the gills.

 

  • Embryonic skin and adult skin bacterial microbiomes differ significantly, which could be due to the special kind of texture of the adult skin that, because of its selective nature, supports a low diversity of bacteria. This needs to be tested though, according to the authors.

 

  • Microbial composition of the surrounding water was distinct from those of other sites of the skates except for two stages: stage 0 and stage 33 when water enters the opening of the egg capsule. The surrounding water mostly does not shape the microbiome structure, although this still calls for further investigation using a deeper sequencing approach.

 

  • A trend of vertical transmission has also been noted for 50% of the adult skin and 25% of the adult gills. And until now this has been the first documentation of vertical transmission in egg-laying Chondrichthyes, report the authors. To some extent  horizontal transmission might also be occurring in these organisms, the exact sources of which remain unidentified. Further, despite sharing the same environment, only six genera of bacteria were found to be shared among the adults, with Unidibacterium being the most prevalent in all of the adult skins and gills.

 

Perspectives with outstanding questions

This study has addressed the idea of microbial transmission in egg-laying marine organisms. Since hatching in skates does not require parental care, it further restricts the possibility for vertical transmission of microbes. In addition, whether horizontal transmission occurs in these skates won’t be very easy to answer as the bacterial community for the surrounding water is distinct from those of the skates. Despite these factors, this study does reveal that both vertical, as well as horizontal transmission of microbes, is possible.

 

This in turn puts forth few other questions:

Which factor is essentially driving the transmission? – would the feeding substrates and any other bottom dwellers closely associated with the skates might be some important sources to look at?

What factors are potentially causing the inter-individual variability and sharing of the limited number of microbes among the individual skates?

Is there any other additional/alternative methods to study the microbial transmissions in such marine organisms?

Tags: chondrichthyes, community ecology, marine organisms, oviparous organisms, skate microbiome

Posted on: 3rd February 2021 , updated on: 8th February 2021

doi: https://doi.org/10.1242/prelights.27265

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Author's response

Katelyn Mika and Alexander Okamoto shared

Thanks for the great writeup and thoughtful questions! We’ve put some of our thoughts on each below.

 

Which factor is essentially driving the transmission? – would the feeding substrates and any other bottom dwellers closely associated with the skates might be some important sources to look at?

In the paper we show that the microbiome of an individual skate is derived both from its mother and the environment. As you read, maternal contributions pass through the egg capsule, but we don’t yet know whether or not this is an active or passive process. As far as environment sources, your guesses are great places to start! Diet almost certainly plays a role, as well as possible seasonal fluctuations in the microbes common in the water column and on the ocean floor. Investigation of other bottom-dwelling marine organisms from the North Atlantic will help us differentiate microbes uniquely enriched in the little skate compared to other species.

What factors are potentially causing the inter-individual variability and sharing of the limited number of microbes among the individual skates?

We expect some level of inter-individual variability given genetic variation among individuals. Additionally, the unique life trajectories of individuals will also lead to differences in microbial acquisition, as is true in humans as well. Our experimental design did not associate egg capsules with the mother, so a future study that tracks microbiome transmission from a female skate to her offspring would offer more precise insights into the fidelity of intergenerational microbial transmission.

Is there any other additional/alternative methods to study the microbial transmissions in such marine organisms?

A major first step will be reproducing these results in other species with alternate life history strategies, such as a shark which gives live birth. Future studies could also focus on other components of the microbiome, such as Archaea and viruses. Other approaches, such as raising skate embryos in sterile seawater or using a fluorescently labeled microbe would allow for more direct identification of where the microbes are coming from.

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