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Eren, A. M.

Publications and source records attributed to Eren, A. M..

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↗

The Ocean Microbiomics Database reveals thermal niches and projected pressure on marine microbes in a warming ocean

Temperature is a key driver of ocean microbial community structure, yet its role in shaping global distributions and their response to warming remains unclear due to fragmented studies, inconsistent methods, and limited environmental context. We present the Ocean Microbiomics Database (OMDB) containing 274,282 genomes forming 31,058 species-level clusters, searchable at https://omdb.microbiomics.io. We show surface temperature is predicted from community composition, driven by thermal niche partitioning among congeneric taxa. Using these thermal niches to model present-day distributions globally, we find that projected warming results in microbial richness declining faster than relative abundance, with losses concentrated at high latitudes and among poorly characterized lineages. Resolving 5,891 species into four thermal clusters reveals ecological structure correlated with genome streamlining, protein thermostability, and marker-gene physicochemistry, enabling prediction of a microorganism's abundance-maximizing temperature directly from its coding sequence. This positions OMDB as a platform spanning molecular traits to global ecology, offering a genome-resolved foundation for understanding how temperature, shown to be a primary driver of ocean microbial life, will continue to shape it as the ocean warms.

microbiology↗

Synteny-aware microbial pangenome graphs reveal blueprints of genomic variation

Pangenomics quantifies the conserved and variable gene repertoire among genomes, but popular implementations ignore gene synteny. Graph-based approaches incorporate both gene homology and synteny, but become difficult to interpret due to pervasive rearrangements. Here we present network-pruning and graph-layout algorithms that enable interactive, synteny-aware quantification and visualization of gene conservation and variability. Applied to 29 genomes of the marine genus Undatipelagibacter (formerly SAR11 subclade Ia.3.VI), we find that genomic variability forms not a few hypervariable islands against a static backbone but a structured continuum, whose variable regions differ in scale, topology, function, and evolutionary character. Genome variation spans from ancient, specialized regions of hundreds of genes whose propensity to vary is conserved across genera, to single hypervariable genes shaped by epistatic co-selection with partners dispersed genome-wide, and shows that chromosomal context carries evolutionary information synteny-unaware pangenomics cannot capture, and some evolutionary processes act on entire functional subsystems throughout a pangenome.

microbiology↗

Amino acid auxotrophy is a feature of a distinct bacterial lifestyle across environments

Amino acid auxotrophy, the loss of biosynthetic potential for an amino acid, is a highly prevalent feature of microbial life, yet the evolutionary processes driving its distribution in nature remain unclear. Here, we sought to determine whether auxotrophy emerges as an independent response to nutrient availability or as part of a broader transition in genomic lifestyle. By first predicting auxotrophies through genome-scale metabolic models and flux-balance analysis, and subsequently applying phylogenetically informed statistical frameworks, we tested the predictions of the Black Queen Hypothesis, which posits that auxotrophy evolves as a dynamic response to metabolite availability, and disentangled the signal of convergent environmental selection from the background of shared evolutionary history. This approach reveals that phylogeny is the dominant predictor of auxotrophy, vastly outweighing environmental context. Beyond correcting for ancestry, our analysis uncovered a previously obscured signal of consistent, co-occurring genomic changes: auxotrophies do not occur as independent losses, but rather as part of a broader reorganization of the genome. We show that auxotrophies co-occur significantly more often than predicted by chance and that the probability of loss scales with the number of other auxotrophies. These findings reveal auxotrophy as a feature of a conserved, phylogenetically entrenched lifestyle rather than a transient response to nutrient availability -- inconsistent with the Black Queen Hypothesis and instead aligning with genome streamlining as the overarching driver of metabolic dependency in natural microbial systems.

evolutionary biology↗

Enrichment of convergent metabolic functions in microbial communities through imposed and emergent environmental niches

Microbial community composition is determined by numerous factors, including environmental filtering, biotic interactions, and stochasticity. Disentangling the relative contribution of these distinct processes is a fundamental problem for microbial ecology. Towards addressing it, here we used controlled experiments on replicate freshwater communities that vary individual factors, and used contig-based metagenomics methods to capture functional composition independently from uneven genome recovery across taxa. After repeated sub-culturing in minimal media lacking organic carbon but containing nitrate and vitamins, communities with distinct initial compositions consistently converged toward similar taxonomic structures and metabolic functions. These included oxygenic photosynthesis and nitrate metabolism, consistent with the imposed growth regime, and also showed reproducible enrichment of anoxygenic photosynthesis, vitamin biosynthesis and degradation pathways. These patterns indicate strong environmental filtering during assembly while also revealing a consistent role for emergent environments arising from microbial activity and metabolic interactions. To more directly test specific environmental drivers, we initiated replicate cultures from a single community and propagated them in the original medium and in variants lacking vitamins or both vitamins and nitrates. Only nitrate removal produced a distinct and statistically significant shift in both composition and function, with nitrate-free communities enriched for cyanobacterial nitrogen fixation and supporting metabolic functions in heterotrophs. Together, these results support a hierarchy of environmental filters determining community outcomes and provide a quantitative framework for predicting and steering community function through rational environmental design.

microbiology↗

Defining the Mycobacterium tuberculosis Pangenome and Suggestions for a New Composite Reference Sequence

Mycobacterium tuberculosis (Mtb) causes tuberculosis (TB), a global disease with diverse clinical and microbiological manifestations. Studies into the biological causes of this phenotypic diversity have been largely limited to a few reference strains. A pangenome approach is likely to provide new insights. Pangenomic tuberculosis studies have been limited the availability of only fragmented genome sequences and error-prone reference genomes. We used a de novo assembly pipeline that generates extremely complete and accurate whole genome sequences to generate 50 closed Mtb genomes across all seven major lineages. We identified 3,377 core gene clusters and 379 accessory clusters. Analysis showed multi-copy core clusters were largely due to gene fragmentation (76%), paralogs (12%), nearly identical gene duplications (4%), or combinations (8%). Sixteen hypervariable regions (HVRs) were identified, including novel paralogs and variable PE/PPE genes. We consolidated these findings into a Pangenome Gene Reference Resource (PGRR) for precision alignment. Our study demonstrates the closed nature of the Mtb pangenome, with most variation in accessory genes and HVRs. The PGRR provides a foundation for improved drug/vaccine target discovery and highlights the need to move beyond the commonly used H37Rv strain to study Mtb genetic and phenotypic diversity. IMPORTANCETuberculosis (TB), caused by Mycobacterium tuberculosis, affects millions globally. Genetic differences among Mtb strains have been difficult to resolve due to incomplete genome references. We sequenced and analyzed complete genomes of 50 Mtb strains from all lineages, identifying 16 hypervariable regions and 3,498 core gene clusters whose diversity mostly stemmed from gene fragmentation, paralog duplication and deletion events and differences in the PE/PPE gene family representation. These differences may explain many of the varied clinical manifestations of TB. We created Pangenome Gene Reference Resource to unify genetic data for precise comparison studies to aid in developing new drugs vaccines and other interventions against this disease.

microbiology↗

A high-resolution diel survey of surface ocean metagenomes, metatranscriptomes, and transfer RNA transcripts

The roles of marine microbes in ecosystem processes are inherently linked to their ability to sense, respond, and ultimately adapt to environmental change. Capturing the nuances of this perpetual dialogue and its long-term implications requires insight into the subtle drivers of microbial responses to environmental change that are most accessible at the shortest scales of time. Here, we present a multi-omics dataset comprising surface ocean metagenomes, metatranscriptomes, tRNA transcripts, and biogeochemical measurements, collected every 1.5 hours for 48 hours at two stations within coastal and adjacent offshore waters of the tropical Pacific Ocean. We expect that this integrated dataset of multiple sequence types and environmental parameters will facilitate novel insights into microbial ecology, microbial physiology, and ocean biogeochemistry and help investigate the different mechanisms of adaptation that drive microbial responses to environmental change.

microbiology↗

Proteobacteria with chemosynthetic potential are highly enriched in the gills of Hypoplectrus reef fishes

A variety of marine invertebrates are known to form associations with chemosynthetic bacteria, but to the best of our knowledge this has not been documented in fishes. Here, we apply genome-resolved metagenomics to the hamlets (Hypoplectrus spp), a model system for the study of speciation in the sea. The analysis of 304 gill samples from 12 hamlet species collected at six locations over 13 years revealed a stark contrast between the gill microbiota and ambient water microbial communities. One novel lineage in the Burkholderiaceae-B family was particularly prevalent across host species, sampling locations and years. Its genome encoded highly complete metabolic modules for carbon fixation and sulfur oxidation, indicating chemosynthetic potential. Its pangenome revealed large-scale geographic structure (western Caribbean, eastern Caribbean and Gulf of Mexico), paralleling the phylogenomic pattern observed in the hamlet radiation. Our survey also identified genomes of multiple novel gill-associated lineages related to known fish gill pathogens, fish gut microbes and free-living seawater taxa. These lineages harbor diverse metabolic modules, involved notably in nitrogen cycling, antibiotic production and biofilm formation, revealing a highly dynamic microbial ecosystem. Overall, our findings suggest complex host-microbe and microbe-microbe eco-evolutionary interactions that may influence fish physiology, homeostasis and immune response.

microbiology↗

Magnimaribacterales marine bacteria genetically partition across the nearshore to open-ocean in the tropical Pacific Ocean

The bacterial order Magnimaribacterales, previously known as the SAR86 lineage, is among the most abundant groups of planktonic bacteria inhabiting the global surface ocean. Despite their prevalence, our understanding of how this genetically diverse lineage partitions into units with coherent ecology and evolution remains limited. Here we surveyed multiple stations in the tropical Pacific Ocean using shotgun metagenomes and 16S rRNA gene amplicons to resolve distinct habitat preferences for Magnimaribacterales lineages across nearshore, offshore, and open-ocean environments. The comprehensive collection of genomes that captured a large fraction of the known evolutionary breadth of Magnimaribacterales, revealed patterns of ecotypic differentiation manifested primarily among genus-level clusters with specific clear preferences for distinct marine habitats. Enrichment analyses identified several functional genes associated with genomes from genera abundant in the nearshore environment, including those associated with sugar metabolism, peptide transport, and glycerophospholipid biosynthesis. Such metabolic adaptations likely facilitate the predominance of specific Magnimaribacterales genera in nearshore environments, promoting ecological partitioning across marine habitats. ImportanceUnderstanding the nature by which abundant, genetically-diverse planktonic marine bacteria organize into evolutionarily related and functionally coherent units remains an important question for scientists interested in the ecology of the global ocean. The bacterial order Magnimaribacterales (formerly SAR86) is one of the most prevalent clades in the global surface ocean, yet its ecological differentiation remains poorly resolved. By integrating metagenomic and amplicon analyses across a nearshore-to-open-ocean gradient in the tropical Pacific, this study reveals distinct habitat preferences within this lineage. The study also highlights how differences in distribution appear are primarily found between genus-level groupings. Our findings also highlight key functional traits, including sugar metabolism and glycerophospholipid biosynthesis, that were associated with the partitioning of nearshore and open-ocean Magnimaribacterales. This work enhances our understanding of the evolutionary processes shaping the diversity of one of the oceans most abundant bacterial clades.

microbiology↗

Assemblies of long-read metagenomes suffer from diverse errors

Genomes from metagenomes have revolutionised our understanding of microbial diversity, ecology, and evolution, propelling advances in basic science, biomedicine, and biotechnology. Assembly algorithms that take advantage of increasingly available long-read sequencing technologies bring the recovery of complete genomes directly from metagenomes within reach. However, assessing the accuracy of the assembled long reads, especially from complex environments that often include poorly studied organisms, poses remarkable challenges. Here we show that erroneous reporting is pervasive among long-read assemblers and can take many forms, including multi-domain chimeras, prematurely circularized sequences, haplotyping errors, excessive repeats, and phantom sequences. Our study highlights the need for rigorous evaluation of the algorithms while they are in development, and options for users who may opt for more accurate reads than shorter runtimes.

bioinformatics↗

Ribosomal protein phylogeography offers quantitative insights into the efficacy of genome-resolved surveys of microbial communities

The increasing availability of microbial genomes is essential to gain insights into microbial ecology and evolution that can propel biotechnological and biomedical advances. Recent advances in genome recovery have significantly expanded the catalogue of microbial genomes from diverse habitats. However, the ability to explain how well a set of genomes account for the diversity in a given environment remains challenging for individual studies or biome-specific databases. Here we present EcoPhylo, a computational workflow to characterize the phylogeography of any gene family through integrated analyses of genomes and metagenomes, and apply this approach to ribosomal proteins to quantify phylogeny-aware genome recovery rates in two genome-resolved investigations of the human gut and oral cavity. Our results demonstrate that EcoPhylo reveals highly resolved, reference-free, multi-domain phylogenies in conjunction with distribution patterns of individual clades across environments, providing a means to assess genome recovery in individual studies and benchmark genome collections.

microbiology↗

Habitat-specificity in SAR11 is associated with a handful of genes under high selection

The order Pelagibacterales (SAR11) is the most abundant group of heterotrophic bacteria in the global surface ocean, where individual sublineages likely play distinct roles in oceanic biogeochemical cycles. Yet, understanding the determinants of niche partitioning within SAR11 has been a formidable challenge due to the high genetic diversity within individual SAR11 sublineages and the limited availability of high-quality genomes from both cultivation and metagenomic reconstruction. Here, we take advantage of 71 new SAR11 genomes from strains we isolated from the tropical Pacific Ocean to evaluate the distribution of metabolic traits across the Pelagibacteraceae, a recently classified family within the order Pelagibacterales encompassing subgroups Ia and Ib. Our analyses of metagenomes generated from stations where the strains were isolated reveals distinct habitat preferences across SAR11 genera for coastal or offshore environments, and subtle but systematic differences in metabolic potential that support these observations. We also observe higher levels of selective forces acting on habitat-specific metabolic genes linked to SAR11 fitness and polyphyletic distributions of habitat preferences and metabolic traits across SAR11 genera, suggesting that contrasting lifestyles have emerged across multiple lineages independently. Together, these insights reveal niche-partitioning within sympatric and parapatric populations of SAR11 and demonstrate that the immense genomic diversity of SAR11 bacteria naturally segregates into ecologically and genetically cohesive units, or ecotypes, that vary in spatial distributions in the tropical Pacific.

microbiology↗

New isolate genomes and global marine metagenomes resolve ecologically relevant units of SAR11

The bacterial order Pelagibacterales (SAR11) is widely distributed across the global surface ocean, where its activities are integral to the marine carbon cycle. High-quality genomes from isolates that can be propagated and phenotyped are needed to unify perspectives on the ecology and evolution of this complex group. Here, we increase the number of complete SAR11 isolate genomes threefold by describing 81 new SAR11 strains from coastal and offshore surface seawater of the tropical Pacific Ocean. Our analyses of the genomes and their spatiotemporal distributions support the existence of 29 monophyletic, discrete Pelagibacterales ecotypes that we define as genera. The spatiotemporal distributions of genomes within genera were correlated at fine scales with variation in ecologically-relevant gene content, supporting generic assignments and providing indications of speciation. We provide a hierarchical system of classification for SAR11 populations that is meaningfully correlated with evolution and ecology, providing a valid and utilitarian systematic nomenclature for this clade.

microbiology↗

Adaptive adjustment of significance thresholds produces large gains in microbial gene annotations and metabolic insights

Gene function annotations enable microbial ecologists to make inferences about metabolic potential from genomes and metagenomes. However, even tools that use the same database and general approach can differ markedly in the annotations they recover. We compare three popular methods for identifying KEGG Orthologs, applying them to genomes drawn from a range of bacterial families that occupy different host-associated and free-living biomes. Our results show that by adaptively tuning sequence similarity thresholds, sensitivity can be substantially improved while maintaining accuracy. We observe the largest improvements when few reference sequences exist for a given protein family, and when annotating genomes from non-model organisms (such as gut-dwelling Lachnospiraceae). Our results suggest that straightforward heuristic adjustments can broadly improve microbial metabolic predictions.

bioinformatics↗

Egoviruses: distant relatives of poxviruses abundant in the gut microbiome of humans and animals worldwide

Large and giant double-stranded DNA viruses are diverse and highly prevalent in the environment where they substantially affect the ecology and evolution of eukaryotes1-4. Until now, they were only sporadically found in the digestive system of vertebrates5-7. Here, we present the discovery of a diversified group of DNA viruses with large linear genomes dubbed egoviruses that comprise a putative viral order most closely related to animal-infecting poxviruses. Egoviruses are found worldwide, almost exclusively in the digestive system of humans, livestock and wild animals. One egovirus is human-specific, evolutionarily constrained, and spread across continents, demonstrating a long-term association between egoviruses and the human population. Analysis of eukaryotic homologs of egovirus core genes suggests that these viruses primarily infect Trichostomatia (Ciliates), which play a central role in ruminant digestive processes8, and Parabasalia (Metamonada), which directly influence animal immunity and gut microbiome ecology9. Egoviruses also contributed to the genetic makeup of polintons, endogenous viruses that proliferated in genomes of Trichomonas vaginalis10 and its close relatives among the Parabasalia. Unlike poxviruses that form brick-shaped virions, egoviruses are predicted to form multilayered icosahedral capsids resembling those of asfuviruses and likely representing the ancestral virion structure. Egoviruses currently are the only known clade of eukaryotic DNA viruses abundant in the animal digestive system. Phylogenomic analysis suggests an evolutionary scenario whereby egovirus-like ancestors of poxviruses infected anaerobic unicellular eukaryotes inside the gut of ancestral animals, before transitioning to animal cell infection which was accompanied by the virion metamorphosis.

microbiology↗

Digital Microbe: A Genome-Informed Data Integration Framework for Collaborative Research on Emerging Model Organisms

The remarkable pace of genomic data generation is rapidly transforming our understanding of life at the micron scale. Yet this data stream also creates challenges for team science. A single microbe can have multiple versions of genome architecture, functional gene annotations, and gene identifiers; additionally, the lack of mechanisms for collating and preserving advances in this knowledge raises barriers to community coalescence around shared datasets. "Digital Microbes" are frameworks for interoperable and reproducible collaborative science through open source, community-curated data packages built on a (pan)genomic foundation. Housed within an integrative software environment, Digital Microbes ensure real-time alignment of research efforts for collaborative teams and facilitate novel scientific insights as new layers of data are added. Here we describe two Digital Microbes: 1) the heterotrophic marine bacterium Ruegeria pomeroyi DSS-3 with >100 transcriptomic datasets from lab and field studies, and 2) the pangenome of the cosmopolitan marine heterotroph Alteromonas containing 339 genomes. Examples demonstrate how an integrated framework collating public (pan)genome-informed data can generate novel and reproducible findings.

bioinformatics↗

Untangling the Role of Pathobionts from Bacteroides Species in Inflammatory Bowel Diseases

Inflammatory bowel diseases (IBD) arise from a convergence of underlying genetic susceptibility, environmental factors, and shifts in gut microbiota function and membership. Although the latter may trigger and contribute to IBD, there is little consensus on a specific causative pathogen. In this study, we demonstrate that commensal Bacteroides fragilis strains from ulcerative colitis (UC) patients before and during the development of ileal pouchitis engraft and promote colitis in specific pathogen free (SPF) IL-10 deficient (IL-10-/-) mice, but not in wild type SPF mice or when mono-associated in germ free mice. The colitis in IL-10-/- mice was also associated with significant alterations in commensal microbiota potentially important for maintaining intestinal and immune homeostasis. UC pouchitis B. fragilis also engrafts in DSS-induced colitis in WT SPF mice, indicating a fitness advantage under conditions of mucosal inflammation over other commensals in the gut microbiota. These findings show that gut inflammation promotes the expansion and fitness of UC-derived Bacteroides species that is associated with changes in the SPF gut microbiota and may be promote colitis in genetically susceptible hosts. ImportanceThis study supports the notion that human inflammatory bowel diseases arise from the emergence of indigenous pathobionts in genetically-prone subjects. Colitis-promoting pathobionts are well-suited to establish themselves in the host inflammatory environment and outcompete endogenous microbiota. Once engrafted, the pathobiont can further aggravate inflammation in a genetically-susceptible host. Such complex interplay among several factors creates a vicious pro-inflammatory cycle and promotes disease development. These findings are consistent with our previous clinical observation that B. fragilis, an otherwise low-abundance commensal species, expands prior to the development of UC pouchitis. We believe these findings are relevant to the pathogenesis of UC pouchitis and possibly human inflammatory bowel diseases in general, underscoring the role of commensal to pathobiont transitions, rather than classical pathogens, in promoting and exacerbating the onset of human IBD.

microbiology↗

A 2-million-year-old microbial and viral communities from the Kap Kobenhavn Formation in North Greenland

Environmental DNA (eDNA) from the 2-million-year-old Kap Kobenhavn Formation of northern Greenland has revealed an ecosystem of plants and animals with no contemporary analogue1. Here, we reconstruct the microbial (bacterial, archaeal, and viral) communities that thrived at the site during this time. By leveraging a novel analytical framework that integrates taxonomic profiling, DNA damage estimates, and functional reconstructions, we identify and distinguish pioneer microbial communities from later permafrost microbial assemblages. We show that at the time of sediment deposition, the terrestrial input at the Kap Kobenhavn site originated from a palustrine wetland, suggesting warmer, non-permafrost conditions. During this period, the detection of methanogenic archaea and signals of their carbon metabolism is consistent with Kap Kobenhavn and similar northern ecosystems contributing moderate methane emissions. Intriguingly, we discover a remarkable nucleotide sequence similarity--exceeding 98%--between pioneer methanogens and present-day analogues in thawing permafrost. This aligns with the concept of "time-traveling" microbes2 surviving across geological time and waiting for conditions to turn favourable rather than evolving to adapt to changing conditions. Importantly, in contrast to the plant and animal communities of the Kap Kobenhavn, a striking similarity in microbial composition to that of a contemporary thawing Arctic suggests that microbial communities may serve as the first indication of broader climate-driven ecosystem disruptions.

microbiology↗