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Biology subjects

Garcia, S. L.

Publications and source records attributed to Garcia, S. L..

At least 19 recordsLinked to original sources

A streamlined and abundant Nitrosopumilus population retains vitamin biosynthesis under high purifying selection in the Baltic Sea

Genome streamlining is expected to favor the loss of costly biosynthetic functions, raising the question of what benefit justifies the continued maintenance of complex pathways in small genomes. Here, we investigated this question in an abundant Nitrosopumilus population from the Baltic Sea that combined a streamlined genome (1.4 Mbp) with substantial biosynthetic capacity for vitamins B1, B7, and B12. We found three lines of evidence that support the biological significance of this retention. First, phylogenomic analysis of 1,077 archaeal species representatives showed that B-vitamin biosynthesis is broadly conserved across ammonia-oxidizing archaea (AOA), indicating maintenance over deep evolutionary timescales. Second, genes associated with B-vitamin biosynthesis tended to be under stronger purifying selection than the genomic background across Baltic Sea metagenomes, consistent with selection preserving these functions in current environmental populations. Third, measurements in the cultured relative Nitrosopumilus maritimus showed B-vitamins and related precursors in both intracellular and extracellular fractions, providing a potential route through which these retained functions could influence metabolite availability beyond the producing cell. Together, our findings suggest that retained biosynthetic pathways in highly streamlined microorganisms reveal functions that are beneficial for the success of a natural population, while also pointing to their potential importance for other community members coexisting within the same environment.

microbiology↗

Baltic Sea microbial cohorts exhibit catabolic specialization and anabolic interdependencies across environmental gradients

Microbial communities are structured by environmental gradients and metabolic interactions, yet the genomic characteristics and metabolic functions of co-occurring populations remain underexplored. Here, we investigated co-occurring microbial cohorts across the Baltic Sea, a system characterized by strong salinity, temperature, and oxygen gradients. For this, we used a genomic catalog consisting of 701 species-representative genomes to recruit reads from 112 metagenomes and infer cohort structure, environmental distributions, and metabolic potential. We identified nine microbial cohorts that showed strong associations with environmental gradients, indicating deterministic assembly. Cohorts differed markedly in genomic traits, with the most abundant and prevalent taxa associated with smaller, streamlined genomes, while a low-oxygen cohort with larger genomes contributed disproportionately to nitrogen and sulfur transformations. Across cohorts, biosynthetic potential was unevenly distributed. Amino acid biosynthesis pathways were frequently complete, whereas B-vitamin pathways were typically incomplete and rarely encoded in full by individual genomes. Metabolites with low pathway completeness showed consistent taxonomic partitioning, with biosynthetic capabilities distributed across taxa rather than collectively encoded within cohorts. Together, these results show that Baltic Sea microbial cohorts are ecologically structured assemblages whose genomic repertoires reflect catabolic specialization and anabolic interdependencies. Our findings highlight microbial cohorts as a useful framework for linking environmental gradients, genome traits, and the organization of metabolic functions in natural microbial communities.

microbiology↗

Widespread potential for phototrophy and convergent reduction of lifecycle complexity in the dimorphic order Caulobacterales

Model bacteria are fundamental for research, but knowledge about their ecology and evolution is often limited. Here we establish evolutionary and ecological context for the model organism Caulobacter crescentus--an alphaproteobacterium intensively studied for its dimorphic lifecycle. By analyzing the species relationships and genetic potential of hundreds of Caulobacterales species, we reveal striking diversity regarding their environmental distribution, morphology, cell development, and metabolism. Our work provides insights into the evolutionary history of morphological features such as the cell curvature determinant crescentin and uncovers a striking case of convergent loss of traits for cellular dimorphism among close relatives of C. crescentus. Moreover, we find that genes for phototrophy are widespread across Caulobacterales and that the new genus Acaudatibacter, described here, includes the first reported Caulobacterales lineage with photoautotrophic potential. Our study advances our understanding of an environmentally widespread bacterial order and sheds light onto the evolution of fundamental prokaryotic features.

microbiology↗

Microbial model communities reveal widespread auxotrophies in abundant bacteria

Microorganisms thrive in complex communities shaped by intricate interactions, yet the extent and ecological implications of biosynthetic dependencies in natural communities remain underexplored. Here, we used a dilution approach to cultivate 204 microbial model communities from the Baltic Sea and recovered 527 metagenome-assembled genomes (MAGs) that dereplicated into 72 species-clusters (>95% average nucleotide identity - ANI). Of these species, at least 70% represent previously uncultivated lineages. Combined with 1073 MAGs from Baltic Sea metagenomes, we generated a genomic catalog of 701 species-clusters. Our results show that cultures with more than 3 species included microorganisms with smaller genome sizes, lower biosynthetic potential for amino acids and B vitamins, and higher prevalence and abundance in the environment. Moreover, biosynthetic genes were distributed across genomes within the same model community, indicating metabolic interdependencies. Our results demonstrate that cultivating bacteria in dilution model communities facilitates access to previously uncultivated but abundant species that likely depend on metabolic partners for survival. Together, our findings highlight the value of community-based cultivation for unraveling ecological strategies. Finally, we confirm that metabolic interdependencies and genome streamlining are widespread features of successful environmental microorganisms.

microbiology↗

The ecological success of freshwater microorganisms is mediated by streamlining and biotic interactions

Genome size is known to reflect aspects of the eco-evolutionary history of prokaryotic species, including their lifestyle, environmental preferences, and habitat breadth. However, it remains uncertain how strongly genome size is linked to microbial prevalence, relative abundance and co-occurrence in the environment. To address this gap, we present a systematic and global-scale evaluation of the relationship between genome size, relative abundance and prevalence in freshwater ecosystems, including 80,561 medium-to-high quality genomes. We identified 9,028 species (defined by ANI >95%) across a manually curated dataset of 636 freshwater metagenomes and calculated their relative abundance. Our results show that prokaryotes with reduced genomes exhibited higher prevalence and relative abundance, and a greater prevalence than expected based on their mean abundance, suggesting that genome streamlining may promote cosmopolitanism. Furthermore, our network analysis revealed that prokaryotes with reduced genomes are found in co-occurrent groups comprising up to 295 species. The species in these groups potentially possess a diminished capacity for synthesizing essential metabolites such as vitamins, amino acids and nucleotides, which may foster complex metabolic interdependencies within the community. Moreover, the fitness advantage of losing biosynthetic functions appears to be frequency dependent: while nucleotide biosynthesis is the most retained biosynthetic function, amino acid and then vitamin biosynthesis are more frequently lost. Our study finds that genome size is linked to microbial community structure and ecological adaptation to freshwaters. Our results underscore genome streamlining as a central ecological and evolutionary strategy that both shapes and is shaped by community dynamics, ultimately fostering interdependences among prokaryotes.

microbiology↗

Profiling trace organic chemical biotransformation genes, enzymes and associated bacteria in microbial model communities

Microbial biotransformation of trace organic chemicals (TOrCs) is an essential process in wastewater treatment for eliminating environmental pollution. Understanding of TOrC biotransformation mechanisms, especially at their original concentrations, is important to optimize treatment performance, whereas our current knowledge is limited. Here we investigated the biotransformation of seven TOrCs by 24 model communities. The genome-centric analyses unraveled the biotransformation drivers concerning functional genes and enzymes and responsible bacteria. We obtained efficient model communities for complete removal on ibuprofen, caffeine and atenolol, and the transformation efficiencies for sulfamethoxazole, carbamazepine, trimethoprim and gabapentin were 0-45%. Biotransformation performance was not fully reflected by the presence of known biotransformation genes and enzymes. However, functional similar homologs to existing biotransformation genes and enzymes (e.g., long-chain-fatty-acid-CoA ligase encoded by fadD and fadD13 gene, acyl-CoA dehydrogenase encoded by fadE12 gene) could play critical roles in TOrC metabolism. Finally, we identified previously undescribed degrading strains, e.g., Rhodococcus qingshengii for caffeine, carbamazepine, sulfamethoxazole and ibuprofen biotransformation, and potential transformation enzymes, e.g., SDR family oxidoreductase targeting sulfamethoxazole and putative hypothetical proteins for caffeine, atenolol and gabapentin biotransformation.

microbiology↗

Bacterial ecology and evolution converge on seasonal and decadal scales

Ecology and evolution are often viewed as distinct processes, which interact on contemporary time scales in microbiomes. To observe these processes in a natural system, we collected a two-decade, 471-sample freshwater lake time series, creating the longest metagenome dataset to date. Among 2,855 species-representative genomes, diverse species and strains followed cyclical seasonal patterns, and one in five species experienced decadal shifts in strain composition. The most globally abundant freshwater bacterium had constant species-level abundance, but environmental extremes appeared to trigger a shift in strain composition and positive selection of amino acid and nucleic acid metabolism genes. These genes identify organic nitrogen compounds as potential drivers of freshwater responses to global change. Seasonal and long-term strain dynamics could be regarded as ecological processes or equivalently as evolutionary change. Rather than as distinct processes that interact, we propose a conceptualization where ecology and evolution converge along a continuum to better describe change in diverse microbial communities.

evolutionary biology↗

Geographic population structure and distinct population dynamics of globally abundant freshwater bacteria

Geographic separation is a principal factor for structuring populations of macroorganisms, with important consequences for evolution, by means of processes such as allopatric speciation. For free-living prokaryotes, implications of geographic separation on their evolution are more unclear. The limited phylogenetic resolution of commonly used markers such as 16S rRNA gene sequences have since long impeded prokaryotic population genetics. However, the vast amount of metagenome sequencing data generated during the last decades from various habitats around the world, now provides an excellent opportunity for such investigations. Here we exploited publicly available and new freshwater metagenomes in combination with genomes of abundant freshwater bacteria to study the impact of geographic separation on population structure. We focused on species that were detected across broad geographic ranges at high enough sequence coverage for meaningful population genomic analyses, i.e. members of the predominant freshwater taxa acI, LD12, Polynucleobacter and Ca. Methylopumilus. Population differentiation increased significantly with spatial distance in all species, but notable dispersal barriers (e.g. oceanic) were not apparent. Yet, the different species showed contrasting rates of geographic divergence and strikingly different population dynamics in time series within individual lakes. While certain populations hardly diverged over several years, others displayed high divergence after merely a few months, similar in scale to populations separated by thousands of kilometers. We speculate that populations with higher strain diversity evolve more monotonously, while low strain diversity enables more drastic clonal expansion of genotypes which will be reflected in strong but transient differentiation between temporally or spatially adjacent populations.

evolutionary biology↗

Network analysis uncovers associations in the turnover of C1 molecules in a winter lake

The generation and consumption of single carbon molecules (CO2 and CH4) by aquatic microbial communities is an essential aspect of the global carbon budget. Organic carbon flow (warm sunlit regimes) is depicted as beginning at the surface with autochthonous fixation followed by biomass settling to sediments, CO2 respiration to the atmosphere, and outflow. We sought to broaden understanding of C1 cycling and consortia by examining the microbial community of a below-ice lake water column in which both input and output are likely disrupted due to ice cover. By analysing the microbial community composition and co-occurrence network of an ice-covered lake timeseries, we were able to identify potential consortia involved in C1 cycling. The network confirmed known associations supporting the efficacy of such analyses but also pointed to previously unknown potential associations. Further and contrary to typical organic carbon flow under warm sunlit regimes, we found support for upward flow of recently fixed carbon in cold low-light conditions under-ice in winter.

microbiology↗

Genome size variation between pelagic and benthic communities across prokaryotic taxonomy and environmental gradients in the Baltic Sea

While theories and models have appeared to explain genome size as a result of evolutionary processes, little work has shown that genome sizes carry ecological signatures. Our work delves into the ecological implications of microbial genome size variation in benthic and pelagic habitats across environmental gradients of the brackish Baltic Sea. While depth is significantly associated with genome size in benthic and pelagic brackish metagenomes, salinity is only correlated to genome size in benthic metagenomes. Overall, we confirm that prokaryotic genome sizes in Baltic sediments (3.47 Mbp) are significantly bigger than in the water column (2.96 Mbp). While benthic genomes have a higher number of functions than pelagic genomes, the smallest genomes coded for a higher number of module steps per Mbp for most of the functions irrespective of their environment. Some examples of this functions are amino acid metabolism and central carbohydrate metabolism. However, we observed that nitrogen metabolism was almost absent in pelagic genomes and was mostly present in benthic genomes. Finally, we also show that Bacteria inhabiting Baltic sediments and water column not only differ in taxonomy, but also in their metabolic potential, such as the Wood-Ljungdahl pathway or the presence of different hydrogenases. Our work shows how microbial genome size is linked to abiotic factors in the environment, metabolic potential and taxonomic identity of Bacteria and Archaea within aquatic ecosystems.

microbiology↗

Genomics of viruses infecting green and purple sulfur bacteria in two euxinic lakes

Viral infections of marine bacteria modulate the rates of primary production and the cycling of organic and inorganic matter in the worlds oceans. Here, we investigated the hypothesis that viral infections influence the ecology of purple and green sulfur bacteria (PSB and GSB) in anoxic and sulfidic (euxinic) lakes, modern analogs of early Earth oceans. Over 200 high and medium quality viral contigs were identified in long-read metagenomes from the sediments and water column of Lime Blue and Poison Lake, respectively. We compared these sequences with 94 predicted prophages identified in the complete genomes of PSB (n = 213) and GSB (n = 33). Viral genomes carrying psbA, encoding the small subunit of photosystem II protein, were present in all three datasets (sediment, water column, and complete genomes). The ubiquity of these genes suggests that PSB and GSB viruses interfere with the light reactions of sulfur-oxidizing autotrophs in a process similar to viral modulation of photosynthesis in Cyanobacteria. Viruses predicted to infect PSB and GSB also encoded auxiliary metabolic genes involved in reductive sulfur assimilation as cysteine, a pathway not yet described in these sulfur bacteria, as well as genes involved in pigment production (crtF) and carbon fixation (CP12, zwf, PGD). These observations highlight the potential for viral modulation of metabolic markers used as proxies to interpret biogeochemical processes in early Earth oceans.

microbiology↗

Taxonomic and functional diversity of aquatic heterotrophs is sustained by dissolved organic matter chemodiversity

Dissolved organic matter (DOM) is ubiquitous in aquatic ecosystems and fundamental for planetary processes and ecosystem functioning. While the link between microbial community composition and heterotrophic utilization of DOM has been recognized, the full diversity of organic compounds, their bioavailability, degradability and specific influences on the diversity and function of heterotrophs are still not clear. Here we experimentally investigate heterotrophic bacteria in thirty-three freshwater model communities. We identified 34 different heterotrophs growing in ambient lake DOM with taxonomic affiliations matching abundant freshwater bacterioplankton. We further describe 25 different heterotrophs growing in the phycosphere of M. Aeruginosa and 6 heterotrophs growing on the DOM produced by M. Aeruginosa with taxonomic affiliation in accord to phycosphere heterotrophs. In our experiment we observed that heterotrophs that live in the phycosphere remove more dissolved organic carbon than abundant freshwater heterotrophs. Moreover, phycosphere heterotrophs have bigger genomes than abundant lake bacteria. Altogether of the 4224 chemical features that were resolved by LC-MS, only 1229 were seen in all three treatments. None of the common/shared compounds were removed across all the model communities, suggesting contrasting niches of the studied taxa. Altogether our study highlights how each model community, with its unique taxonomic assemblages and organotroph functioning is upkept by the chemodiversity of DOM.

ecology↗

Biogenic methane cycling is controlled by microbial cohorts

The generation and consumption of methane by aquatic microbial communities is an important contribution to the global carbon budget. We sought to broaden understanding of consortia members and interactions by combining multiple methods including analysis of natural and cultivated microbial communities. By analysing the microbial community composition and co-occurrence patterns of a lake time-series we were able to identify potential consortia involved in methane cycling. In combination with methane flux, we also analysed the community composition and co-occurrence patterns of reduced microbial model communities with inoculum from the same lake. While the network analyses confirmed many known associations, when combined with results from mixed cultures, we noted new players in methane cycling. Cultivated model communities were shown to be an effective method to explore the rarer but still important players in methane cycling and for identifying new putative members. Here we show that using multiple methods to approach the complex problem of methane cycling consortia yields not just insights into the known taxa but highlights potential new members creating new hypotheses to be tested.

microbiology↗

Comprehensive analysis of chemical and biological problems associated with browning agents used in aquatic studies

Inland waters receive and process large amounts of colored organic matter from the terrestrial surroundings. These inputs dramatically affect the chemical, physical, and biological properties of water bodies, as well as their roles as global carbon sinks and sources. To understand the complex changes associated with allochthonous inputs, experiments are needed. However, manipulative studies, especially at ecosystem scales, require large amounts of dissolved organic matter with optical and chemical properties resembling indigenous organic matter. Here we compared the chemical and biological impacts of two leonardite products (HuminFeed (HF) and SuperHume (SH)) and a freshly derived reverse osmosis concentrate of organic matter (RO) in a set of comprehensive mesocosm- and laboratory-scale experiments and analyses. The chemical properties of RO concentrate and the leonardite products were very different with leonardite products being low and RO being high in carboxylic functional groups. Light had a strong impact on the properties of leonardite products, including loss of color and increased particle formation. Furthermore, HF had drastic impacts on bacteria as light stimulated bacterial production and modified community composition, while dark conditions appeared to inhibit bacterial processes. While none of the browning agents inhibited the growth of the tested phytoplankton, Gonyostomum semen, leonardite products had detrimental effects on zooplankton abundance and Daphnia reproduction. We conclude that the effects of browning agents extracted from leonardite are in sharp contrast to those originating from terrestrially-derived DOM. Hence, they should be used with great caution in experimental studies on the consequences of terrestrial carbon for aquatic systems.

ecology↗

A genomic perspective on genome size distribution across Earth's microbiomes reveals a tendency to gene loss

Our view of genome size in Archaea and Bacteria has remained skewed as the data used to paint its picture has been dominated by genomes of microorganisms that can be cultivated under laboratory settings. However, the continuous effort to catalog the genetic make-up of Earths microbiomes specifically propelled by recent extensive work on uncultivated microorganisms, provides a unique opportunity to revise our perspective on genome size distribution. Capitalizing on a recently released extensive catalog of tens of thousands of metagenome-assembled genomes, we provide a comprehensive overview of genome size distributions. We observe that the known phylogenetic diversity of environmental microorganisms possesses significantly smaller genomes than the collection of laboratory isolated microorganisms. Aquatic microorganisms average 3.1 Mb, host-associated microbial genomes average 3.0 Mb, terrestrial microorganism average 3.7 Mb and isolated microorganisms average 4.3 Mb. While the environment where the microorganisms live can certainly be linked to genome size, in some cases, evolutionary phylogenetic history can be a stronger predictor. Moreover, ecological strategies such as auxotrophies have a direct impact on genome size. To better understand the ecological drivers of genome size, we expand on the known and the overlooked factors that influence genome size in different environments, phylogenetic groups and trophic strategies.

microbiology↗

Comprehensive dataset of shotgun metagenomes from stratified freshwater lakes and ponds

Stratified lakes and ponds featuring steep oxygen gradients are significant net sources of greenhouse gases and hotspots in the carbon cycle. Despite their significant biogeochemical roles, the microbial communities, especially in the oxygen depleted compartments, are poorly known. Here, we present a comprehensive dataset including 267 shotgun metagenomes from 41 stratified lakes and ponds mainly located in the boreal and subarctic regions, but also including one tropical reservoir and one temperate lake. For most lakes and ponds, the data includes a vertical sample set spanning from the oxic surface to the anoxic bottom layer. The majority of the samples were collected during the open water period, but also a total of 29 samples were collected from under the ice. In addition to the metagenomic sequences, the dataset includes environmental variables for the samples, such as oxygen, nutrient and organic carbon concentrations. The dataset is ideal for further exploring the microbial taxonomic and functional diversity in freshwater environments and potential climate change impacts on the functioning of these ecosystems.

ecology↗

Freshwater Chlorobia exhibit metabolic specialization among cosmopolitan and endemic populations

Photosynthetic bacteria from the class Chlorobia (formerly phylum Chlorobi) sustain carbon fixation in anoxic water columns. They harvest light at extremely low intensities and use various inorganic electron donors to fix carbon dioxide into biomass. Until now, most information on their functional ecology and local adaptations came from isolates and merely 26 sequenced genomes that are poor representatives of natural populations. To address these limitations, we analyzed global metagenomes to profile planktonic Chlorobia cells from the oxyclines of 42 freshwater bodies, spanning subarctic to tropical regions and encompassing all four seasons. We assembled and compiled over 500 genomes, including metagenome-assembled genomes (MAGs), single-cell genomes (SAGs), and reference genomes from cultures, clustering them into 71 metagenomic operational taxonomic units (mOTUs) or "species". Of the 71 mOTUs, 57 were classified as genus Chlorobium and these mOTUs varied in relative abundance up to ~60% of the microbial communities in the sampled anoxic waters. Several Chlorobium-associated mOTUs were globally distributed whereas others were endemic to individual lakes. Although most clades encoded the ability to oxidize hydrogen, many were lacking genes for the oxidation of specific sulfur and iron substrates. Surprisingly, one globally distributed Scandinavian Chlorobium clade encoded the ability to oxidize hydrogen, sulfur, and iron, suggesting that metabolic versatility facilitated such widespread colonization. Overall, these findings provide new insights into the biogeography of the Chlorobia and the metabolic traits that facilitate niche specialization within lake ecosystems. ImportanceThe reconstruction of genomes from metagenomes has enabled unprecedented insights into the ecology and evolution of environmental microbiomes. We applied this powerful approach to 274 metagenomes collected from diverse freshwater habitats that spanned oxic and anoxic zones, sampling seasons, and latitudes. We demonstrate widespread and abundant distributions of planktonic Chlorobia-associated bacteria in hypolimnetic waters of stratified freshwater ecosystems and pinpoint nutrients that likely fuel their electron chains. Being photoautotrophs, these Chlorobia organisms also have the potential to serve as carbon sources that support metalimnetic and hypolimnetic food webs.

ecology↗

Streamlined freshwater bacterioplankton Nanopelagicales (acI) and Ca. Fonsibacter (LD12) thrive in functional cohorts

While fastidious microbes can be abundant and ubiquitous in their natural communities, many fail to grow axenically in laboratories due to auxotrophies or other dependencies. To overcome auxotrophies these microbes rely on their surrounding cohort. A cohort may consist of kin (ecotypes) or more distantly related organisms (community) with the cooperation being reciprocal or non-reciprocal, and expensive (Black Queen hypothesis) or costless (byproduct). These metabolic partnerships (whether at single species population or community level) enable dominance by and coexistence of these lineages in nature. Here we examine the relevance of these cooperation models to explain the abundance and ubiquity of the dominant fastidious bacterioplankton of a dimictic mesotrophic freshwater lake. Using both culture dependent (minimalist mixed cultures) and culture independent (SSU rRNA gene time series and environmental metagenomics) methods we independently identified the primary cohorts of Actinobacterial genera "Ca. Planktophila" (acI-A) and "Ca. Nanopelagicus" (acI-B), and the Proteobacterial genus "Ca. Fonsibacter" (LD12). While "Ca. Planktophila" and "Ca. Fonsibacter" had no correlation in their natural habitat, they have the potential to be complementary in laboratory settings. We also investigated the bi-functional catalase-peroxidase enzyme KatG (a common good which "Ca. Planktophila" is dependent upon) and its most likely providers in the lake. Further we found that while ecotype and community cooperation combined may explain "Ca. Planktophila" population abundance, the success of "Ca. Nanopelagicus" and "Ca. Fonsibacter" is better explained as a community byproduct. Ecotype differentiation of "Ca. Fonsibacter" as a means of escaping predation was supported but not for overcoming auxotrophies. IMPORTANCEThis study examines evolutionary and ecological relationships of three of the most ubiquitous and abundant freshwater bacterial genera: "Ca. Planktophila" (acI-A), "Ca. Nanopelagicus" (acI-B), and "Ca. Fonsibacter" (LD12). Due to high abundance, these genera might have a significant influence on nutrient cycling in freshwaters worldwide and this study adds a layer of understanding to how seemingly competing clades of bacteria can co-exist by having different cooperation strategies. Our synthesis ties together network and ecological theory with empirical evidence and lays out a framework for how the functioning of populations within complex microbial communities can be studied.

microbiology↗