Motile bacteria leverage bioconvection for eco-physiological benefits in a natural aquatic environment.

Introduction: Bioconvection, a phenomenon characterized by the collective upward swimming of motile microorganisms, has mainly been investigated within controlled laboratory settings, leaving a knowledge gap regarding its ecological implications in natural aquatic environments. This study aims to address this question by investigating the influence of bioconvection on the eco-physiology of the anoxygenic phototrophic sulfur bacteria community of meromictic Lake Cadagno. Methods: Here we comprehensively explore its effects by comparing the physicochemical profiles of the water column and the physiological traits of the main populations of the bacterial layer (BL). The search for eco-physiological effects of bioconvection involved a comparative analysis between two time points during the warm season, one featuring bioconvection (July) and the other without it (September). Results: A prominent distinction in the physicochemical profiles of the water column centers on light availability, which is significantly higher in July. This minimum threshold of light intensity is essential for sustaining the physiological CO2 fixation activity of Chromatium okenii, the microorganism responsible for bioconvection. Furthermore, the turbulence generated by bioconvection redistributes sulfides to the upper region of the BL and displaces other microorganisms from their optimal ecological niches. Conclusion: The findings underscore the influence of bioconvection on the physiology of C. okenii and demonstrate its functional role in improving its metabolic advantage over coexisting phototrophic sulfur bacteria. However, additional research is necessary to confirm these results and to unravel the multiscale processes activated by C. okenii's motility mechanisms.

Bacterial, Phytoplankton, and Viral Distributions and Their Biogeochemical Contexts in Meromictic Lake Cadagno Offer Insights into the Proterozoic Ocean Microbial Loop.

Lake Cadagno, a permanently stratified high-alpine lake with a persistent microbial bloom in its chemocline, has long been considered a model for the low-oxygen, high-sulfide Proterozoic ocean. Although the lake has been studied for over 25 years, the absence of concerted study of the bacteria, phytoplankton, and viruses, together with primary and secondary production, has hindered a comprehensive understanding of its microbial food web. Here, the identities, abundances, and productivity of microbes were evaluated in the context of Lake Cadagno biogeochemistry. Photosynthetic pigments together with 16S rRNA gene phylogenies suggest the prominence of eukaryotic phytoplankton chloroplasts, primarily chlorophytes. Chloroplasts closely related to those of high-alpine-adapted Ankyra judayi persisted with oxygen in the mixolimnion, where photosynthetic efficiency was high, while chloroplasts of Closteriopsis-related chlorophytes peaked in the chemocline and monimolimnion. The anoxygenic phototrophic sulfur bacterium Chromatium dominated the chemocline along with Lentimicrobium, a genus of known fermenters. Secondary production peaked in the chemocline, which suggested that anoxygenic primary producers depended on heterotrophic nutrient remineralization. The virus-to-microbe ratio peaked with phytoplankton abundances in the mixolimnion and were at a minimum where Chromatium abundance was highest, trends that suggest that viruses may play a role in the modulation of primary production. Through the combined analysis of bacterial, eukaryotic, viral, and biogeochemical spatial dynamics, we provide a comprehensive synthesis of the Lake Cadagno microbial loop. This study offers a new ecological perspective on how biological and geochemical connections may have occurred in the chemocline of the Proterozoic ocean, where eukaryotic microbial life is thought to have evolved. IMPORTANCE As a window into the past, this study offers insights into the potential role that microbial guilds may have played in the production and recycling of organic matter in ancient Proterozoic ocean chemoclines. The new observations described here suggest that chloroplasts of eukaryotic algae were persistent in the low-oxygen upper chemocline along with the purple and green sulfur bacteria known to dominate the lower half of the chemocline. This study provides the first insights into Lake Cadagno's viral ecology. High viral abundances suggested that viruses may be essential components of the chemocline, where their activity may result in the release and recycling of organic matter. The integration of diverse geochemical and biological data types provides a framework that lays the foundation to quantitatively resolve the processes performed by the discrete populations that comprise the microbial loop in this early anoxic ocean analogue.

Mixotrophic Growth Under Micro-Oxic Conditions in the Purple Sulfur Bacterium "Thiodictyon syntrophicum".

The microbial ecosystem of the meromictic Lake Cadagno (Ticino, Swiss Alps) has been studied intensively in order to understand structure and functioning of the anoxygenic phototrophic sulfur bacteria community living in the chemocline. It has been found that the purple sulfur bacterium "Thiodictyon syntrophicum" strain Cad16T, belonging to the Chromatiaceae, fixes around 26% of all bulk inorganic carbon in the chemocline, both during day and night. With this study, we elucidated for the first time the mode of carbon fixation of str. Cad16T under micro-oxic conditions with a combination of long-term monitoring of key physicochemical parameters with CTD, 14C-incorporation experiments and quantitative proteomics using in-situ dialysis bag incubations of str. Cad16T cultures. Regular vertical CTD profiling during the study period in summer 2017 revealed that the chemocline sank from 12 to 14 m which was accompanied by a bloom of cyanobacteria and the subsequent oxygenation of the deeper water column. Sampling was performed both day and night. CO2 assimilation rates were higher during the light period compared to those in the dark, both in the chemocline population and in the incubated cultures. The relative change in the proteome between day and night (663 quantified proteins) comprised only 1% of all proteins encoded in str. Cad16T. Oxidative respiration pathways were upregulated at light, whereas stress-related mechanisms prevailed during the night. These results indicate that low light availability and the co-occurring oxygenation of the chemocline induced mixotrophic growth in str. Cad16T. Our study thereby helps to further understand the consequences micro-oxic conditions for phototrophic sulfur oxidizing bacteria. The complete proteome data have been deposited to the ProteomeXchange database with identifier PXD010641.

Effect of organic carbon and metal accumulation on the bacterial communities in sulphidogenic sediments.

A unique geochemical setting in Lake Cadagno, Switzerland, has led to the accumulation of insoluble metal sulphides in the sedimentary record as the result of past airborne pollution. This offers an exceptional opportunity to study the effect of these metals on the bacterial communities in sediments, and in particular to investigate further the link between metal contamination and an increase in the populations of endospore-forming bacteria observed previously in other metal-contaminated sediments. A decrease in organic carbon and total bacterial counts was correlated with an increase in the numbers of endospores in the oldest sediment samples, showing the first environmental evidence of a decrease in nutrient availability as a trigger of sporulation. Proteobacteria and Firmicutes were the two dominant bacterial phyla throughout the sediment, the former in an area with high sulphidogenic activity, and the latter in the oldest samples. Even though the dominant Firmicutes taxa were stable along the sediment core and did not vary with changes in metal contamination, the prevalence of some molecular species like Clostridium sp. was positively correlated with metal sulphide concentration. However, this cannot be generalized to all endospore-forming species. Overall, the community composition supports the hypothesis of sporulation as the main mechanism explaining the dominance of endospore formers in the deepest part of the sediment core, while metal contamination in the form of insoluble metal sulphide deposits appears not to be linked with sporulation as a mechanism of metal tolerance in this sulphidogenic ecosystem.