Sunday, May 5, 2024

Microbe Spotlight #2 : The Chilean Thioploca "Supercolony"


TLDR; Giant sulfide-oxidizing mats comprise the largest microbial habitat on Earth and may have been more ecologically-dominant prior to the emergence of animals.

     Lately, I've been hearing about some interesting findings off the coast of Chile. Apparently, the continental shelf is home to a extensive microbial mat that covers an area roughly the size of Greece, making it the largest macroscopic assemblage of microorganisms on the planet. The mats themselves resemble shag rugs, comprised of colorless filaments which poke out of the sediment. For this reason, fishermen in the region have given the mats the name "estopa", in reference to the Spanish word for unwashed wool or flax.

   As for the true identity of these mats, the filaments are comprised of a common marine bacterium known as Thioploca. Thioploca are members of the family Thiotrichaceae; a group which contains sulfide-oxidizing giants, such as Thiomargarita magnifica (an organism which currently holds the title for the word's largest prokaryote) and Beggiatoa (which can be found in a host of freshwater environments).



       (Left) A close-up image of some Thioploca filaments swaying in the current. 

(Right) "Estopa" as seen from further away. 

     Interestingly, all of these organisms are faced with a similar dilemma. In short, they rely upon sulfide deep within the sediment for energy and nitrate at the surface of the sediment as an electron acceptor. As a result, these microbes have had to get rather clever.

     For example, the Beggiatoa are composed of massive, multicellular filaments which glide up and down through the substrate, much like how a whale might breach the surface of the ocean for a gulp of air before returning back to the depths in order to hunt for krill. 

     In addition, the interior of their cells are mostly comprised of large hollow vacuoles which contain massive stockpiles of nitrate harvested from the surface. In this way, the Beggiatoa are able to "hold their breath", thereby allowing them to carry out respiration deep beneath the sediment where nitrate is scarce. In contrast, Thioploca use a slightly different approach.

     Both Beggiatoa and Thioploca are multicellular and contain nitrate vacuoles. However, Instead of simply traveling up and down through the sediment, the Thioploca filaments band together and construct large protective sheaths. These sheaths can grow to lengths of 5-10 centimeters and serve as "elevators"; offering direct passage from the sulfidic sediments below to the oxic-zone above.

     These sheaths are also well-fortified and can have walls as thick as 1.5 milimeters, making them readily visible to the naked eye. This seems to suggest that the sheaths play an additional role in offering protection from microbial competitors.


                 
                (Top) Diagram of a Thioploca colony (Bottom) Image of Thioploca auaucae filaments emerging from the opening of a sheath. 

     However, the extracellular polymers comprising the sheaths are highly nutritious and tend to attract a host of scavengers. As a result, these structures have to be constantly maintained, lest the become overrun by hungry microbes looking for a meal. 

     In addition, the sheaths also appear to provide protection for a host of other organisms as well, forming a unique microbial consortium. Some of these "endobionts"  live amongst the Thioploca, reducing the sulfate they exhale and converting back to sulfide. In this way, they are able to recycle sulfur and convert it into a form that the Thioploca can use, thereby helping them grow (This is especially useful in sheaths containing high-densities of Thioploca where there is significantly more competition for sulfide.) Meanwhile, others reside within abandoned sheaths and take them over, much like how a hermit crab will make use of an abandoned shell.



 (Above) A Thioploca Sheath, containing a 1-milimeter-long filamentous endobiont 
(Highlighted through fluorescent labeling)

     With that said, we're still left with the question of why so much Thioploca exist along the Chilean coast. In order to understand this, we first need to understand upwelling.

     As winds travel along the coast, surface waters are deflected out to sea, creating a vacuum that encourages the upwelling of nutrient-rich water from below. This circulation transports nutrients and organic carbon deposited within deeper sediments to the coast, triggering massive blooms of phytoplankton. These phytoplankton eventually exhaust all of the available resources and sink to the ocean floor. This then results in marine decomposers exhausting all the available oxygen and cause rising euxinia (water chemistry characterized by low oxygen levels and high sulfide concentrations). 

     These conditions provide an ideal home for the Thioploca that is full of sulfide and free from large grazing animals. With that said, it's interesting to speculate on whether these sorts of ecosystems could have been much more widespread prior to the emergence of animals, rather than appearing at just a few sites scattered across the globe as they do today.

     Throughout the Archean and Proterozoic, coastal microbial mats would be far more numerous than their modern-day counterparts due to the absence of grazing and burrowing animals. Some of this material would have become swept up by the currents and transported into deeper waters, leading to the formation of massive offshore depositional habitats, such as those preserved in the 2.1 billion-year-old Gunflint Formation of Northern Ontario. Furthermore, a lack of bioturbation (burrowing) in deeper waters would allow this organic detritus to consolidate and develop vast communities of decomposers, thereby triggering euxinia. This in turn would allow organisms with similar lifestyles to Thioploca and Beggiotoa to thrive.

     Who knows, perhaps we've stumbled upon evidence for these ancient communities already.

     Within the Gunflint Formation, chert deposits have been found to be rich in tubular sheaths known as Gunflintia. While we don't know their precise identity, they are typically interpreted as belonging to dead cyanobacteria that were carried into deeper waters and partially consumed by various scavengers. However, it's not improbable to suggest that the filaments may have once belonged to the Thiotrichaceae and could have been the ancient relatives of modern-day Thioploca. However, this is all just speculation for now.


(Left) A light microscopy image and some 3D-reconstructions of Gunflintia fossils, taken 
from the Gunflint Formation. 
(Right) Gunflintia fossils with spheres of pyrite embedded within them (Shown in orange). These were likely produced as sulfate-reducing scavengers consumed the sheaths and produced sulfide, which would have then reacted with ferric iron in the sediment to form small granules containing pyrite and other FeS minerals.

Side note : While writing this article, it also occurred to me that similar ecosystems might become especially prominent on habitable exoplanets where animal analogues never arise, such as in the case of Leeuwenhoek (a fictional world that I hope to feature in my upcoming book).


Citations :

https://schaechter.asmblog.org/schaechter/2010/09/commuting-to-work.html

https://www.researchgate.net/publication/240675026_Benthos_communities_in_oxygen_deficient_shelf_and_upper_slope_areas_of_the_Peruvian_and_Chilean_Pacific_coast_and_changes_caused_by_El_Nino 

https://www.youtube.com/watch?v=_IdFXLS9msM

https://www.pnas.org/doi/10.1073/pnas.1221965110


Also, here's some footage of the Thioploca and Beggiotoa that have shown up in some of my cultures :

https://youtube.com/clip/UgkxM12xI17VMARJ6wVzrUeSb9tGc-k6m8jz?si=d_sySiwgaXFBgvmH

https://youtube.com/clip/UgkxB0-EatXJ7KTS4W9PAv8c28ZLbuVGyk1b?si=nl7lAVR_lLizhZ3c

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