Why is Lake Cadagno so special? This water body’s notable characteristic is its permanent stratification separating the mixolimnion, composed of crystal clear, oxygenated water, like any alpine lake, from the monimolimnion rich in dissolved salts and completely anoxic. A chemocline with a high concentration of ions in the lower part maintains the separation between the two layers. The chemocline is also characterized by opposite gradients in redox potential (ORP) with oxygen, which tends to zero, and sulfide, which increases with depth (up to 3.0 mg l− 1)35. This redox-stratified structure makes Lake Cadagno a useful analogous environment for the study of biogeochemical cycles in the early Earth37–40. In fact, anoxygenic microorganisms found in the depths of the lake are potentially very similar to the primordial life forms that appeared on our planet and gave rise to the evolutionary process that is still ongoing. In the sediment and deepest dark zones, the SRB’s anoxygenic sulfur-based chemoheterotrophic metabolism allows them to thrive41. At the same time, in the lower part of the chemocline illuminated by the light, sulfur bacteria rely on a photoautotrophic metabolism42. At the upper part of the chemocline, in the presence of little oxygen, blue-green algae (BGA), precursors to the appearance of oxygen about 2.0 billion years ago, can be found42.
The meromictic Lake Cadagno is also known for an intriguing layer located in the lower part of the chemocline, which hosts a dense community, up to 107 cells ml− 1 in the “warm season”, of anoxygenic phototrophic sulfur bacteria28,43. This community is concentrated in a small portion of the lake, about 1.0 m immediately, forming a so-called bacterial layer (BL; turbidity > 10 FTU). The BL zone is inhabited by a very heterogeneous community of anoxygenic phototrophic sulfur bacteria that share the same ecological niche using different evolutionary strategies. Here, we can find at least 7 species of purple (PSB) and 2 of green (GSB)sulfur bacteria44. PSB, round-shaped microorganisms with the ability to store sulfur globules inside the cell, are present with two different phenotypes, namely large-celled Chromatium okenii that actively swims thanks to a tuft of flagella45 and small-celled PSB (six other species) that usually form aggregates and passively float in the water thanks to gas vacuoles34,46. GSB, two species of Chlorobium29, are small rectangular shaped that do not store sulfur globules inside their cells. The pigment apparatus of the latter, which composes the photosynthetic antenna, is more sensitive to low light intensity than PSB, allowing them to survive deeper in the water column47. The photosynthetic activity of PSB and GSB is also different, relying on photosystem II and the Calvin cycle and photosystem I and reductive inverse tricarboxylic acid, respectively. To summarize, the BL comprises of different populations of anoxygenic phototrophic sulfur bacteria that have developed different evolutionary strategies to survive in the same ecological niche.
In this study, we analyze the intra- and inter-seasonal stability of the water column stratification and the BL dynamics for three years. The dynamics of the three main populations (with different phenotypes), of the BL were monitored by sampling at varying depth points during the “warm season”, from June to October of years 2019, 2020 and 2021. As previously suggested31, the large-cell PSB C. okenii dominance in terms of cells number is observed in the summer months (Fig. 4B). As autumn approaches and the intensity and duration of sunlight hours naturally reduce, a change in the BL community happens, with a reduction in C. okenii and an increase in other small-cell PSB, particularly GSB (Fig. 4B). Moreover, it is well known that GSB have an advantage over PSB at low light intensities47. In any case, in 2020 an extreme event in late August (Aug. 30, 2021) changed the position of the BL, effectively increasing the amount of light that allowed C. okenii to continue to be the most abundant population (Fig. 4C). While in 2021, an extremely wet summer greatly reduced the dynamism of the BL (Fig. 4D). If we consider the total biovolume (Fig. 4A), it becomes extremely clear that PSB C. okenii is the most important population of BL due to the significant size difference of the three microorganisms considered, with C. okenii (63.3 µm3) 15 and 76 times more voluminous than T. syntrophicum (4.2 µm3) and C. phaeobacteroides (0.8 µm3), respectively. Our findings highlight the complexity of the physical and microbiological interaction that mediates the dominance of species at the seasonal time scale.
Interestingly, the period of C. okenii is most abundant coincides with the presence of bioconvection32. C. okenii actively swims toward the light by means of flagella and stops in the presence of oxygen, determining a local increase in the number of cells. This builds up the density of the water in that area, generating a macroscopic (bio)convective motion that creates a well-mixed layer of up to 1 m thickness48,49. Surprisingly, C. okenii keeps its upward migration at night, maintaining bioconvection even in the absence of light33, possibly following gravity thanks to internal granules. The deepening of the BL, combined with shorter daylight hours and generally less sunny weather, probably results in insufficient sunlight reaching the BL, reducing the energy available to sustain active cell movement50.
We have just shown that the BL community has been affected by abiotic events related to the meteorological situation. However, have the stability of the meromixis and the structure of the lake also been impacted? One way to estimate the stability of the water column of a lake is through the Schmidt stability index, which determines the energy required to mix the water column fully51,52. During the 3 years of monitoring, the value remained constant at 175 ± 0.02 kJ m− 2, about 10 times higher than for lakes of similar size53. As long as the two-layer structure is maintained, this lake will remain a unique hotspot for these anoxygenic microorganisms and a place to study the earliest life forms on Earth. Given the growing concern about climate change54,55, as average temperatures rise and extreme weather events become more frequent, is there a potential risk to the meromixis of Lake Cadagno? Looking to the past, the physical stratification and the anoxygenic microorganisms have persisted for more than 10,000 years25. There has been a steady increase in average temperatures over the past 50 years, which has a pronounced effect on sub-alpine regions, such as the Piora Valley. Data collected over the past 30 years, from 1985 to 2021 (Fig. 5), shows relatively stable temperature (Fig. 5A) and conductivity (Fig. 5C) characteristics in the water column, which are then also reflected in the elevated and constant Schmidt stability index (Fig. 5B). The gradual air temperature increase from current anthropologically driven climate change seems not expected to break the meromictic structure56, which also survived the thermal oscillations of the Holocene57. However, it is so far not clear how climate change, induced hydrological variations, will affect salt-rich groundwater inflow and SO42− discharge in the deep water, which is then converted to H2S by the SRBs, an essential for the development of the BL at the chemocline. Such changes in groundwater flow and composition would profoundly affect the water column stability of the system. Further research is required to assess the effect that climate change might have on the biotic-abiotic interactions maintaining the influx of H2S, which is necessary for BL survival.
Normally, PSB and GSB communities are strongly dependent on euxinic conditions and light availability. PSB are highly responsive to variations in light intensity and, consequently, more vulnerable to situations that increase the turbidity or decrease the depth of the chemocline. The pigments found in the sediments demonstrate that the BL community underwent many changes throughout the past 12,500 years24,25,56. In this regard, it is interesting to note that the H2S concentration profile underwent a major change at the beginning of the century (Fig. 5D). In 2000 a violent hurricane named Lothar caused a partial mixing of the lake that altered the turbidity and light profiles, with the latter reduced by 10 times at the level of the BL 58. This change in the water column led to a substantial increase in the number of cells in the BL due to the development of a "new" previously absent species of GSB, Chlorobium chlatratiforme29,44. The reduction in sulfide concentration observed in Fig. 5D is probably related to the increase in the number of cells in the BL from 106 to 107. During the regular monitoring of Lake Cadagno, other unusual occurrences were observed that affected the BL community, but without being related to changes in H2S concentration. For example, in 2017 an exceptionally hot and windless summer led to an anomalous BGA-PC bloom just above the BL that caused a reduced light penetration31. And finally, during our study, we observed the effect of exceptional weather conditions, such as the extremely cold and rainy summer of 2021. The lack of good weather, and thus sunshine, led to a marked reduction in the concentration of phototrophic bacteria populations in BL.
In conclusion, as supported by previous research, this study emphasizes the significance of the coexistence of abiotic and biotic factors in the development and maintenance of a specific ecosystem. Our observations highlight a direct relationship between weather and BL development and proliferation, especially at an intra-sesonal level. However, upon examining the past 12,500 years and the last 30 years, we can argue that the future of this proxy for early life on Earth seems safe. Although climate change can affect the long term inter-seasonal composition of the BL community, mainly through extreme wind-related phenomena29,44,58, there is no indication of changes in the stability of the stratification. Lake Cadagno has maintained its meromictic state over the past three decades, featuring a persistent anoxygenic monimolimnion while recording only minor changes in the Schmidt stability index. If global warming continues or exacerbates, the supply of salt-rich water from sublacustrine springs might decrease, leading to a potential water scarcity issue. To avoid further speculations, we recommend measuring the yearly dynamics of H2S in the deep waters, its interaction with salt-rich groundwater recharge and how changes in rainfall and snowpack will affect groundwater flow into Lake Cadagno.