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Pinhassi, J.

Publications and source records attributed to Pinhassi, J..

10 recordsLinked to original sources

Temperature and dissolved organic matter shape marine prokaryotic activity and gene expression in a sub-arctic sea

Temperature and dissolved organic matter (DOM) are important drivers of microbial activity, but their effects, alone or in combination, on the physiological responses of sub-arctic prokaryotic assemblages remain poorly understood. In a northern Baltic Sea one-month mesocosm experiment, we therefore exposed a coastal microbial community to temperature and nutrient regimes representative of winter and early summer (i.e., 1{degrees}C and 10{degrees}C, with and without DOM additions) in a 2x2 factorial design. Midway through the experiment, specific growth rates were highest for the 10{degrees}C plus DOM treatment (TN; [~]2.5 day-1), comparable for the 1{degrees}C plus DOM (N) and the 10{degrees}C (T) treatments at [~]1.0 day-1; and low for the control (1{degrees}C, no DOM enrichment [C]; 0.2 day-1). Taxonomic analysis of metatranscriptomes uncovered broad treatment specific responses, and a PERMANOVA on the 182,618 transcribed genes revealed statistically significant effects of both temperature and DOM, and significant interaction effects between the two (altogether involving 18% of genes). Significant differences in transcription identified by EdgeR analysis included Nitrosopumilus genes for ammonium uptake and ammonia oxidation in the 1{degrees}C mesocosms (C, N), membrane transporters for small organic acids in the N-treatment, genes for nitrogen and phosphorus assimilation along with molecular chaperones in the T-treatment, and dominance of Oceanospirillales genes for energy and growth metabolism in the TN-treatment. These metatranscriptomic responses were associated with changes in e.g. prokaryotic growth rates and growth efficiency, providing clues to how successional changes in community composition and metabolism are directed by temperature and DOM as central factors underlying environmental change. ImportanceIt is recognized that increases in temperature and dissolved organic matter loading are key to understanding how climate change will influence polar ecosystems. Still, little is known of the effects of these factors on the physiological responses of Arctic prokaryotes. Since prokaryotes are principal drivers of biogeochemical cycles, we investigated how temperature and dissolved organic matter influence prokaryotic transcriptional responses in taxonomy and metabolic pathways. The metatranscriptomics analyses uncovered broad treatment specific responses linked with changes in prokaryotic community composition, growth rates, and growth efficiency. Yet, and importantly, the expression of most metabolic functions remained stable, suggesting a pronounced functional resilience of the prokaryotic community enabled by shifts in the dominance of different taxa. This emphasizes the large potential and importance of identifying the metabolic functions that underlie the divergence of prokaryotic communities in response to environmental changes projected to alter some of the most vulnerable marine environments.

ecology↗

Experimental assessment of marine microbial interactions: from predatory protists promoting bacterial survival to bacterial lysis of the protists

Bacteria in aquatic environments are a principal food source for predatory protists. Whereas interactions between bacteria and protists are recognized to play important roles in determining the pathogenesis and epidemiology of several human pathogens, few studies have systematically characterized the interactions between specific aquatic bacteria and protists beyond the prey-predator relation. We therefore surveyed the outcome of individual co-cultures between 18 different genome-sequenced marine bacteria with known virulence gene repertoires and three model protist species widely used for assessing bacteria-protist interactions. Strikingly, ten, five, and three bacterial isolates were capable of lysing the protists Acanthamoeba polyphaga, Tetrahymena pyriformis and Euglena gracilis, respectively. A majority of the bacteria were able to grow and/or maintain viable populations in the presence of viable protists. Some bacteria survived longer in the presence of viable protists but not heat-killed protists, and were observed in protist vacuoles. In this respect, thus, marine bacteria are similar to several protist-dependent human pathogens, including Legionella. Analyses of growth patterns in low-nutrient media showed that co-cultivation with A polyphaga allowed one bacterial strain to overcome nutritional stress and obtain active growth. Five isolates depended on viable amoebae to grow, notwithstanding nutrient media status. The remarkable capability of surviving encounters with, and even actively killing, bacterivorous protists, indicates that diverse (and possibly novel) bacterial defense strategies and virulence mechanisms to access nutrients are widespread among marine bacteria. The diversity of interactions uncovered here has important implications for understanding ecological and evolutionary consequences of population dynamics in bacteria and protists. IMPORTANCEThe microbiome constitutes the base of food webs in marine waters. Its composition partly reflects biotic interactions, where bacteria primarily are considered as prey of predatory protists. However, studies that focus on one or a few species have shown that some bacteria have abilities to escape grazing and may even be capable of lysing their protist predators. In this study, we substantially extend these findings by systematically investigating interactions among multiple taxa of both bacteria and protists. Our results show that marine bacteria display a wider and more complex range of interactions with their predators than generally recognized - from growth dependency to protist lysis. Given that such interactions play key roles in the pathogenesis and epidemiology of several human pathogens, our findings imply that bacterial virulence traits can contribute to defining the structure and ecology of the marine microbiome.

microbiology↗

Quantification of metabolic niche occupancy dynamics in a Baltic Sea bacterial community

Progress in molecular methods has enabled the monitoring of bacterial populations in time. Nevertheless, understanding community dynamics and its links with ecosystem functioning remains challenging due to the tremendous diversity of microorganisms. Conceptual frameworks that make sense of time-series of taxonomically-rich bacterial communities, regarding their potential ecological function, are needed. A key concept for organizing ecological functions is the niche, the set of strategies that enable a population to persist and define its impacts on the surroundings. Here we present a framework based on manifold learning, to organize genomic information into potentially occupied bacterial metabolic niches over time. We apply the method to re-construct the dynamics of putatively occupied metabolic niches using a long-term bacterial time-series from the Baltic Sea, the Linnaeus Microbial Observatory (LMO). The results reveal a relatively low-dimensional space of occupied metabolic niches comprising groups of taxa with similar functional capabilities. Time patterns of occupied niches were strongly driven by seasonality. Some metabolic niches were dominated by one bacterial taxon whereas others were occupied by multiple taxa, and this depended on season. These results illustrate the power of manifold learning approaches to advance our understanding of the links between community composition and functioning in microbial systems. ImportanceThe increase in data availability of bacterial communities highlights the need for conceptual frameworks to advance our understanding of these complex and diverse communities alongside the production of such data. To understand the dynamics of these tremendously diverse communities, we need tools to identify overarching strategies and describe their role and function in the ecosystem in a comprehensive way. Here, we show that a manifold learning approach can coarse grain bacterial communities in terms of their metabolic strategies and that we can thereby quantitatively organize genomic information in terms of potentially occupied niches over time. This approach therefore advances our understanding of how fluctuations in bacterial abundances and species composition can relate to ecosystem functions and it can facilitate the analysis, monitoring and future predictions of the development of microbial communities.

microbiology↗

Warmer temperatures favor slower-growing bacteria in natural marine communities

Earths life-sustaining oceans harbor diverse bacterial communities that display varying composition across time and space. While particular patterns of variation have been linked to a range of factors, unifying rules are lacking, preventing the prediction of future changes. Here, analyzing the distribution of fast- and slow-growing bacteria in ocean datasets spanning seasons, latitude, and depth, we show that higher seawater temperatures universally favor slower-growing taxa, in agreement with theoretical predictions. Our results explain why slow growers dominate at the ocean surface, during summer, and near the tropics, and provide a framework to understand how bacterial communities will change in a warmer world.

ecology↗

Abundance and expression of hgcAB genes and mercury availability jointly explain methylmercury formation in stratified brackish waters

Neurotoxic methylmercury (MeHg) is formed by microbial methylation of inorganic divalent Hg (HgII) and constitutes severe environmental and human health risks. The methylation is enabled by hgcA and hgcB genes, but it is not known if the associated molecular-level processes are rate-limiting or enable accurate prediction of MeHg formation in nature. In this study, we investigated the relationships between hgcA genes and MeHg across redox stratified water columns in the brackish Baltic Sea. We found that the abundance of hgcA genes and transcripts combined with the concentration of dissolved HgII-sulfide species were strong predictors of both HgII methylation rate and MeHg concentration, implying their roles as principal joint drivers of MeHg formation in these systems. In establishing relationships between hgcA genes and MeHg, we advance the fundamental understanding of mechanistic principles governing MeHg formation in nature and enable refined predictions of MeHg levels in coastal seas in response to the accelerating spread of oxygen deficient zones.

ecology↗

Taxon-specific shifts in bacterial and archaeal transcription of dissolved organic matter cycling genes in a stratified fjord

A considerable fraction of organic matter derived from photosynthesis in the euphotic zone settles into the oceans interior, and under way is degraded by diverse microbial consortia that utilize a suite of extracellular enzymes and membrane transporters. Still, the molecular details that regulate carbon cycling across depths remain little explored. As stratification in fjords has made them attractive models to explore patterns in biological oceanography, we here analyzed bacterial and archaeal transcription in samples from five depth layers in the Gullmar Fjord, Sweden. Transcriptional variation over depth correlated with gradients in chlorophyll a and nutrient concentrations. Differences in transcription between sampling dates (summer and early autumn), were strongly correlated with ammonium concentrations, which potentially was linked with a stronger influence of (micro-)zooplankton grazing in summer. Transcriptional investment in carbohydrate-active enzymes (CAZymes) decreased with depth and shifted toward peptidases, partly a result of elevated CAZyme transcription by Flavobacteriales, Cellvibrionales and Synechococcales at 2-25 m and a dominance of peptidase transcription by Alteromonadales and Rhodobacterales from 50 m and down. In particular, CAZymes for chitin, laminarin, and glycogen were important. High levels of transcription of ammonium transporters by Thaumarchaeota at depth (up to 18% of total transcription), along with the genes for ammonia oxidation and CO2-fixation, indicated that chemolithoautotrophy contributed to the carbon flux in the fjord. The taxon-specific expression of functional genes for processing of the marine DOM pool and nutrients across depths emphasizes the importance of different microbial foraging mechanisms across spatiotemporal scales for shaping biogeochemical cycles. IMPORTANCEIt is generally recognized that stratification in the ocean strongly influences both the community composition and the distribution of ecological functions of microbial communities, which in turn are expected to shape the biogeochemical cycling of essential elements over depth. Here we used metatranscriptomics analyses to infer molecular detail on the distribution of gene systems central to the utilization of organic matter in a stratified marine system. We thereby uncovered that pronounced shifts in transcription of genes encoding CAZymes, peptidases, and membrane transporters occurred over depth among key prokaryotic orders. This implies that sequential utilization and transformation of organic matter through the water column is a key feature that ultimately influences the efficiency of the biological carbon pump.

ecology↗

Picozoa are archaeplastids without plastid

The endosymbiotic origin of plastids from cyanobacteria gave eukaryotes photosynthetic capabilities and launched the diversification of countless forms of algae. These primary plastids are found in members of the eukaryotic supergroup Archaeplastida. All known archaeplastids still retain some form of primary plastids, which are widely assumed to have a single origin. Here, we used single-cell genomics from natural samples combined with phylogenomics to infer the evolutionary origin of the phylum Picozoa, a globally distributed but seemingly rare group of marine microbial heterotrophic eukaryotes. Strikingly, the analysis of 43 single-cell genomes shows that Picozoa belong to Archaeplastida, specifically related to red algae and the phagotrophic rhodelphids. These picozoan genomes support the hypothesis that Picozoa lack a plastid, and further reveal no evidence of an early cryptic endosymbiosis with cyanobacteria. These findings change our understanding of plastid evolution as they either represent the first complete plastid loss in a free-living taxon, or indicate that red algae and rhodelphids obtained their plastids independently of other archaeplastids.

evolutionary biology↗

Divergent gene expression responses in two Baltic Sea heterotrophic model bacteria to dinoflagellate dissolved organic matter

Phytoplankton release massive amounts of dissolved organic matter (DOM) into the water column during recurring blooms in coastal waters and inland seas. The released DOM encompasses a complex mixture of both known and unknown compounds, and is a rich nutrient source for heterotrophic bacteria. The metabolic activity of bacteria during and after phytoplankton blooms can hence be expected to reflect the characteristics of the released DOM. We therefore investigated if bacterioplankton could be used as "living sensors" of phytoplankton DOM quantity and/or quality, by applying gene expression analyses to identify bacterial metabolisms induced by DOM. We used transcriptional analysis of two Baltic Sea bacterial isolates (Polaribacter sp. BAL334 [Flavobacteriia] and Brevundimonas sp. BAL450 [Alphaproteobacteria]) growing with DOM from axenic cultures of the dinoflagellate Prorocentrum minimum. We observed pronounced differences between the two bacteria both in bacterial growth and the expressed metabolic pathways in cultures exposed to dinoflagellate DOM compared with controls. Differences in metabolic responses between the two isolates were caused both by differences in gene repertoire between them (e.g. in the SEED categories for membrane transport, motility and photoheterotrophy) and the regulation of expression (e.g. fatty acid metabolism), emphasizing the importance of separating the responses of different taxa in analyses of community sequence data. Similarities between the bacteria included substantially increased expression of genes for Ton and Tol transport systems in both isolates, which are commonly associated with uptake of complex organic molecules. Polaribacter sp. BAL334 showed stronger metabolic responses to DOM harvested from exponential than stationary phase dinoflagellates (128 compared to 26 differentially expressed genes), whereas Brevundimonas sp. BAL450 responded more to the DOM from stationary than exponential phase dinoflagellates (33 compared to 6 differentially expressed genes). These findings suggest that shifts in bacterial metabolisms during different phases of phytoplankton blooms can be detected in individual bacterial species and can provide insights into their involvement in DOM transformations.

microbiology↗

Marine snow as a habitat for microbial mercury methylators in the Baltic Sea

Methylmercury (MeHg), a neurotoxic compound biomagnifying in aquatic food webs, can be a threat to human health via fish consumption. However, the composition and distribution of the microbial communities mediating the methylation of mercury (Hg) to MeHg in marine systems remain largely unknown. In order to fill this gap of knowledge, we used the Baltic Sea Reference Metagenome (BARM) dataset to study the distribution of the genes involved in Hg methylation (the hgcAB gene cluster). We determined the relative abundance of the hgcAB genes and their taxonomic identity in 81 brackish metagenomes that cover spatial, seasonal and redox variability in the Baltic Sea water. The hgcAB genes were predominantly detected in anoxic water, but some hgcAB genes were also detected in hypoxic and normoxic waters. Higher relative quantities of hgcAB genes were found in metagenomes from marine snow compared to free-living communities in anoxic water, suggesting that marine snow are hotspot habitats for Hg methylators in oxygen-depleted seawater. Phylogenetic analysis identified well-characterized Hg methylators such as Deltaproteobacteria in oxygen-depleted water, but also uncovered Hg methylators within the Spirochaetes and Lentisphaerae phyla. Altogether, our work unveils the diversity of the microorganisms mediating MeHg production in the Baltic Sea and pinpoint the ecological niches of these microorganisms within the marine water column.

microbiology↗

Genomes from uncultivated prokaryotes: a comparison of metagenome-assembled and single-amplified genomes

BackgroundProkaryotes dominate the biosphere and regulate biogeochemical processes essential to all life. Yet, our knowledge about their biology is for the most part limited to the minority that has been successfully cultured. Molecular techniques now allow for obtaining genome sequences of uncultivated prokaryotic taxa, facilitating in-depth analyses that may ultimately improve our understanding of these key organisms.\n\nResultsWe compared results from two culture-independent strategies for recovering bacterial genomes: single-amplified genomes and metagenome-assembled genomes. Single-amplified genomes were obtained from samples collected at an offshore station in the Baltic Sea Proper and compared to previously obtained metagenome-assembled genomes from a time series at the same station. Among 16 single-amplified genomes analyzed, seven were found to match metagenome-assembled genomes, affiliated with a diverse set of taxa. Notably, genome pairs between the two approaches were nearly identical (>98.7% identity) across overlapping regions (30-80% of each genome). Within matching pairs, the single-amplified genomes were consistently smaller and less complete, whereas the genetic functional profiles were maintained. For the metagenome-assembled genomes, only on average 3.6% of the bases were estimated to be missing from the genomes due to wrongly binned contigs; the metagenome assembly was found to cause incompleteness to a higher degree than the binning procedure.\n\nConclusionsThe strong agreement between the single-amplified and metagenome-assembled genomes emphasizes that both methods generate accurate genome information from uncultivated bacteria. Importantly, this implies that the research questions and the available resources are allowed to determine the selection of genomics approach for microbiome studies.

bioinformatics↗