The relevance of PSB C. okenii for the ecology and biogeochemistry of Lake Cadagno has been well described in previous studies showing for instance that with a total biovolume of 1.8 × 107 µm3 mL-1 it contributed approximately 40% to the total ammonium uptake and 70% to the inorganic carbon uptake (53).
With the present study, I evidenced and supported the specific role and significance of C.
okenii in the ecosystem of the chemocline. FCM identification of C. okenii allowed its quantification at high spatial and temporal resolution in the chemocline, revealing for instance
that C. okenii is probably driving the generation of a mixed layer with homogeneous temperature and conductivity gradients in the chemocline (Chapter 4).
This process called bioconvection, previously limited to laboratory observations, has been observed and described in a natural environment, i.e. Lake Cadagno, for the first time in the frame of my work (88). The underlying mechanisms were confirmed by findings from laboratory experiments, and are based on motile C. okenii cells accumulating at the upper chemocline of Lake Cadagno. This accumulation substantially increases the local density of the water column, which eventually become unstable and break up into characteristics plumes, thus initiating bioconvection. The study presented in Chapter 4 (88), successfully combined biological analysis of cell densities and physico-chemical surveys with mathematical simulation of the phenomenon.
However, further studies are required to understand the consequences of bioconvection on microenvironment, on the microbial community, and in general on the biogeochemical implications for the lake ecosystem. Given the size of the water volume affected in a zone of steep physico-chemical gradients, bioconvection might be of high relevance for ecophysiological conditions of the microbial community with ecosystem scale consequences, including proliferation, germination, nutrient uptake, gas transport and primary production (177–179).
Moreover, particularly in the natural environment, bioconvection also represents an understudied but potentially important mechanism influencing the vertical distribution, and consequently growth and productivity, of the microbial community. Bioconvection might also be important in shaping inter-specific interactions and mid- to long-term dynamics in the microbial community (discussed above). For instance, it seems that bioconvection comprises a competitive advantage for C. okenii that overcompensates the substantial energy expenditure from swimming against gravity.
In Chapter 1 and Chapter 2, I monitored the seasonal occurrence of large-celled PSB C.
chemocline occurred at the same time as the mixed layer, which was particularly evident in mid to late-summer (Chapter 4). This observation lends further support to the hypothesized relevance of bioconvection in promoting an advantage for C. okenii against other phototrophic sulfur populations. Consequently, bioconvection could be the dominant evolutionary mechanism increasing the competitive advantage of C. okenii against microbial taxa with higher affinity to light and H2S such as GSB (139) or with ability to fix CO2 both in the light and dark such as Candidatus “T. syntrophicum” (55). Furthermore whereas GSB of the Chlorobiaceae family are strict anaerobes, members of PSB can be microaerobic and even anaerobic (180). This characteristic could underly the competitive advantage of bioconvection for C. okenii because it is able exploit the novel niche created by bioconvection to increase its activity, in particular when oxidizing sulfide under anoxic as well as microoxic conditions.
Besides phototrophic growth, complete genome analysis of another member of the Chromatiaceae, i.e. PSB Allochromatium vinosum revealed its capacity to grow chemotrophically with low concentration of oxygen as an electron acceptor (181). Draft genome analysis of C. okenii using RAST SEED Viewer (comparative genomic tool, S. Lüdin unpublished) reveals the presence of an extended respiration electron accepting system with two terminal cytochrome d ubiquinol oxidases and two terminal cytochrome oxidases, as well as a subsystem for biogenesis of c-type cytochromes. Therefore, it might be assumed that through its motility, C. okenii has the ability to physically link photosynthetic anoxic sulfide oxidation at the bottom of the mixed layer in the chemocline with chemotrophic sulfide oxidation at its top. This metabolic flexibility may give advantages to C. okenii in fitness and growth rates over non-motile phototrophic sulfur bacteria in the chemocline.
The vertical expansion of C. okenii habitat created through bioconvection might be significant not only at level of interspecific interactions and competition, but also for intraspecific interactions. Quorum sensing (QS) might be relevant for inter- and intraspecific interactions. QS
represents a system of stimulus and response correlated with density of bacterial populations and relies on the ability of its members to communicate by using chemical signals such as acylated homoserine lactones (AHLs) (182,183). The steps involved in detecting and responding to fluctuations in cell numbers are analogous in all known quorum-sensing systems. Low molecular weight molecules known as autoinducers are synthesized intracellularly and passively released or actively secreted to the environment. As the number of cells in a population increases, the extracellular concentration of autoinducer also increases. Cognate receptors bind the autoinducers once they reached the minimal threshold level required for detection and signal transduction cascades, resulting in population-wide changes in gene expression (184). This QS-coordinated gene-regulation system thus controls QS-coordinated behavior of bacterial communities, and in the case of C. okenii motility might be influenced in response to cell density. Seasonal increase of C. okenii density in early to mid-summer might stimulate QS, causing the population to migrate and expand the habitat. With a positive feedback, this process could augment population fitness by allowing for extra population growth.
In addition to interactions within the chemocline, bioconvection significantly influences the surrounding environment in the oxic-anoxic transition zone. Consequences of this process may include alterations of trophic interactions that are relevant for other compartments of the lake ecosystem. In particular, at the upper limit of the chemocline, grazing by zooplankton and interactions with other organism groups such as the phytoplankton species Cryptomonas phaseolus (7) or cyanobacteria (Chapter 1) might be affected.