Biology subjects

Tonolla, M.

Publications and source records attributed to Tonolla, M..

4 recordsLinked to original sources

bioRxiv2021

Bacterial, phytoplankton, and viral dynamics of 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 anoxic chemocline, has long been considered a model for the low-oxygen, high-sulfide Proterozoic ocean where early microbial life gave rise to Earths oxygenated atmosphere. 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. Photo-synthetic pigments and chloroplast 16S rRNA gene phylogenies suggested high abundances of eukaryotic phytoplankton, primarily Chlorophyta, through the water column. Of these, a close relative of Ankyra judayi, a high-alpine adapted chlorophyte, peaked with oxygen in the mixolimnion, while Closteriopsis-related chlorophytes peaked in the chemocline and monimolimnion. Anoxygenic phototrophic sulfur bacteria, Chromatium, dominated the chemocline along with Lentimicrobium, a newly observed genus of known fermenters. Secondary production peaked in the chemocline, suggesting anoxygenic primary producers depended on heterotrophic nutrient remineralization. Virus-to-microbe ratios spanned an order of magnitude, peaking with high phytoplankton abundances and at a minimum at the peak of Chromatium, dynamic trends that suggest viruses may play a role in the modulation of oxygenic and anoxygenic photo- and chemosynthesis in Lake Cadagno. Through the combined analysis of bacterial, eukaryotic, viral, and biogeochemical dynamics of Lake Cadagno, this study provides a new perspective on the biological and geochemical connections that comprised the food webs of the Proterozoic ocean. IMPORTANCEAs a window to the past, the study offers insights into the role of microbial guilds of Proterozoic ocean chemoclines in the production and recycling of organic matter of sulfur- and ammonia-containing ancient oceans. The new observations described here suggest that eukaryotic algae were persistent in the low oxygen upper-chemocline in association with purple and green sulfur bacteria in the lower half of the chemocline. Further, this study provides the first insights into Lake Cadagno viral ecology. High viral abundances suggested viruses may be essential components of the chemocline where their activity may result in the release and recycling of organic matter. The framework developed in this study through the integration of diverse geochemical and biological data types lays the foundation for future studies to quantitatively resolve the processes performed by discrete populations comprising the microbial loop in this early anoxic ocean analogue.

microbiology↗

bioRxiv2021

Microbial loop of Proterozoic ocean analogue

Meromictic Lake Cadagno, an ancient ocean analogue, is known for its permanent stratification and persistent anoxygenic microbial bloom within the chemocline. Although the anaerobic microbial ecology of the lake has been extensively studied for at least 25 years, a comprehensive picture of the microbial food web linking the bacterial layer to phytoplankton and viruses, with explicit measures of primary and secondary production, is still missing. This study sought to better understand the abundances and productivity of microbes in the context of nutrient biogeochemical cycling across the stratified zones of Lake Cadagno. Photosynthetic pigments and chloroplast 16S rRNA gene phylogenies suggested the presence of eukaryotic phytoplankton through the water column. Evidence supported high abundances of Ankyra judayi, a high-alpine adapted chlorophyte, in the oxic mixolimnion where oxygenic-primary production peaked. Through the no- and low-oxygen chemocline and monimolimnion, chlorophytes related to Closteriopsis acicularis, a known genus of meromictic lakes, and Parachlorella kessleri were observed. Chromatium, anoxygenic phototrophic sulfur bacteria, dominated the chemocline along with Lentimicrobium, a genus of known fermenters whose abundance was newly reported in Lake Cadagno. Secondary production peaked in the chemocline suggesting primary producers depend on hetrotrophs for nutrient remineralization. As previously observed, sulfur reducing bacteria (SRBs), especially Desulfocapsa and Desulfobulbus, were present in the chemocline and anoxic monimolimnion. Virus-to-microbe ratios (VMR) peaked in the zone of phytoplankton, yet were at a minimum at the peak of Chromatium. These dynamic trends suggest viruses may play a role in the modulation of oxygenic and anoxygenic photo- and chemosynthesis in Lake Cadagno and other permanently stratified systems. ImportanceAs a window to the past, the study offers insights into the role of microbial guilds of Proterozoic ocean chemoclines in the production and recycling of organic matter of sulfur- and ammonia-containing ancient oceans. The new observations described here suggest that eukaryotic algae were persistent in the low oxygen upper-chemocline in association with purple and green sulfur bacteria in the lower half of the chemocline. Further, this study provides the first insights into Lake Cadagno viral ecology. High viral abundances suggested viruses may be essential components of the chemocline where their activity may result in the release and recycling of organic matter. The framework developed in this study through the integration of diverse geochemical and biological data types lays the foundation for future studies to quantitatively resolve the processes performed by discrete populations comprising the microbial loop in this early anoxic ocean analogue.

microbiology↗

bioRxiv2018

Dark aerobic sulfide oxidation by anoxygenic phototrophs in the anoxic waters of Lake Cadagno

SUMMARYAnoxygenic phototrophic sulfide oxidation by green and purple sulfur bacteria (PSB) plays a key role in sulfide removal from anoxic shallow sediments and stratified waters. Although some PSB can also oxidize sulfide with nitrate and oxygen, little is known about the prevalence of this chemolithotrophic lifestyle in the environment. In this study, we investigated the role of these phototrophs in light-independent sulfide removal in the chemocline of Lake Cadagno. Our temporally resolved, high-resolution chemical profiles indicated that dark sulfide oxidation was coupled to high oxygen consumption rates of ~9 M O2{middle dot}h-1. Single-cell analyses of lake water incubated with 13CO2 in the dark revealed that Chr. okenii was to a large extent responsible for aerobic sulfide oxidation and it accounted for up to 40 % of total dark carbon fixation. The genome of Chr. okenii reconstructed from the Lake Cadagno metagenome confirms its capacity for microaerophilic growth and provides further insights into its metabolic capabilities. Moreover, our genomic and single-cell data indicated that other PSB grow microaerobically in these apparently anoxic waters. Altogether, our observations suggest that aerobic respiration may not only play an underappreciated role in anoxic environments, but also that organisms typically considered strict anaerobes may be involved.\n\nORIGINALITY-SIGNIFICANCE STATEMENTThis study reveals that dark aerobic sulfide oxidation within an anoxic layer dominated by anoxygenic phototrophic bacteria in the stratified water column of Lake Cadagno is to a large extent carried out by the anoxygenic phototrophic bacterium Chromatium okenii. Our findings imply that aerobic metabolisms may be more prevalent in anoxic zones than previously thought. We also present an environmental metagenome-assembled genome of Chr. okenii which is the first genome sequence for the genus Chromatium and reveals new interesting physiological features of this environmentally relevant organism, including its capacity for aerobic respiration.

microbiology↗

bioRxiv2018

Anoxygenic Photosynthesis and Dark Carbon Metabolism under micro-oxic conditions in the Purple Sulfur Bacterium \"Thiodictyon syntrophicum\" nov. strain Cad16T

1.The microbial ecosystem of the meromictic Lake Cadagno (Ticino, Swiss Alps) has been studied intensively to understand metabolic functions driven by the highly abundant anoxygenic phototrophic sulfur bacteria of the families Chromatiaceae and Chlorobiaceae. It was found that the sequenced isolate \"Thiodictyon syntrophicum\" nov. sp. str. Cad16T, belonging to the Chromatiaceae, may fix 26% of all bulk inorganic carbon in the chemocline at day and night. With this study, we elucidated the mode of dark carbon fixation of str. Cad16T with a combination of long-term monitoring of key physicochemical parameters with CTD, 14C-incorporation experiments and quantitative proteomics of in situ dialysis bag incubations of pure 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 in September. While CO2 assimilation rates were higher during the light period, the relative change in the proteome (663 quantified proteins) was only 1% of all CDS encoded in str. Cad16T. Oxidative respiration was thereby upregulated at light, whereas stress-related mechanisms prevailed during the night. These results indicate that the low light availability due to high cell concentrations and the oxygenation of the chemocline induced a mixotrophic growth in str. Cad16T.\n\nThe complete proteome data have been deposited to the ProteomeXchange with identifier PXD010641.

microbiology↗