Search bioRxiv⌕ Search

Biology subjects

Storelli, N.

Publications and source records attributed to Storelli, N..

6 recordsLinked to original sources

Synergistic phenotypic shifts during domestication promote plankton-to-biofilm transition in purple sulfur bacterium Chromatium okenii

The ability to isolate microorganisms from natural environments to pure cultures under optimized laboratory settings has markedly improved our understanding of microbial ecology. Laboratory-induced artificial growth conditions often diverge from those in natural ecosystems, forcing wild isolates into selective pressures which are distinct compared to those in nature. Consequently, fresh isolates undergo diverse eco-physiological adaptations mediated by modification of key phenotypic traits. For motile microorganisms, we still lack a biophysical understanding of the relevant traits which emerge during domestication, and possible mechanistic interrelations between them which could ultimately drive short-to-long term microbial adaptation under laboratory conditions. Here, using microfluidics, atomic force microscopy (AFM), quantitative imaging, and mathematical modelling, we study phenotypic adaptation of natural isolates of Chromatium okenii, a motile phototrophic purple sulfur bacterium (PSB) common to meromictic settings, grown under ecologically-relevant laboratory conditions over multiple generations. Our results indicate that the naturally planktonic C. okenii populations leverage synergistic shifts in cell-surface adhesive interactions, together with changes in their cell morphology, mass density, and distribution of intracellular sulfur globules, to supress their swimming traits, ultimately switching to a sessile lifeform under laboratory conditions. A computational model of cell mechanics confirms the role of the synergistic phenotypic shifts in suppressing the planktonic lifeform. Over longer domestication periods ([~]10 generations), the switch from planktonic to sessile lifeform is driven by loss of flagella and enhanced adhesion. By investigating key phenotypic traits across different physiological stages of lab-grown C. okenii, we uncover a progressive loss of motility via synergistic phenotypic shifts during the early stages of domestication, which is followed by concomitant deflagellation and enhanced surface attachment that ultimately drive the transition of motile sulphur bacteria to a sessile biofilm state. Our results establish a mechanistic link between suppression of motility and surface attachment via synergistic phenotypic changes, underscoring the emergence of adaptive fitness under felicitous laboratory conditions that comes at a cost of lost ecophysiological traits tailored for natural environments. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=85 SRC="FIGDIR/small/563228v1_ufig1.gif" ALT="Figure 1"> View larger version (33K): org.highwire.dtl.DTLVardef@fcb6b0org.highwire.dtl.DTLVardef@13e18d0org.highwire.dtl.DTLVardef@1cf3ee6org.highwire.dtl.DTLVardef@12a837b_HPS_FORMAT_FIGEXP M_FIG C_FIG

biophysics↗

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

Bioconvection, the active self-sustaining transport phenomenon triggered by the accumulation of motile microbes under competing physico-chemical cues, has been long studied, with recent reports suggesting its role in driving ecologically-relevant fluid flows. Yet, how this collective behaviour impacts the ecophysiology of swimming microbes remains unexplored. Here, through physicochemical profiles and physiological characterizations analysis of the permanently stratified meromictic Lake Cadagno, we characterize the community structure of a dense layer of anaerobic phototrophic sulfur bacteria, and report that the associated physico-chemical conditions engender bioconvection when bulk of the motile purple sulfur bacterium Chromatium okenii synchronize their movement against the gravity direction. The combination of flow cytometry and fluorescent in situ hybridization (FISH) techniques uncover the eco-physiological effects resulting from bioconvection, and simultaneous measurements using dialysis bags and 14C radioisotope, allowed us to quantify in situ the diurnal and nocturnal CO2 fixation activity of the three co-existing species in the bacterial layer. The results provide a direct measure of the cellular fitness, with comparative transcriptomics data - of C. okenii populations present in regions of bioconvection vis-a-vis populations in bioconvection-free regions - indicating the transcripts potentially involved in the bioconvection process. This work provides direct evidence of the impact of bioconvection on C. okenii metabolism, and highlights the functional role of bioconvection in enhancing the metabolic advantage of C. okenii relative to other microbial species inhabiting the microbial layer.

microbiology↗

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↗

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↗

Molybdate to prevent the formation of sulfide during the process of biogas production

The process of anaerobic digestion producing biogas is an eco-friendly energy source that promotes recycling from waste biomass such as food chain residues, wet waste, wastewater. In this study, we focused on the problem of the sulfide (H2S) produced by the sulfate-reducing bacteria (SRB) in the presence of sulfate residues. This byproduct is dangerous for human health and an issue due to the highly corrosive effect on metallic components. To this purpose, the Molybdate, a sulfate analog, known in the literature to inhibit SRBs by blocking the first enzyme of the metabolic pathway of anaerobic respiration, was applied. The experiments carried out showed that a concentration of 0.3 mM of molybdate was enough to inhibit the SRB in a complex environment of the anaerobically digested sludge (ADS) took from a real biogas producing bioreactor. During the study, we observed the importance of the sulfate concentration sulfate in the system. Indeed, the production of sulfide was stopped only under the threshold ratio value of 1:10 (molybdate: sulfate). In the short term, the addition of molybdate did not alter the production and quality (% of methane) of the biogas, nor the anaerobic microbial community, including SRB population itself.

microbiology↗

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↗