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Aylward, F. O.

Publications and source records attributed to Aylward, F. O..

At least 19 recordsLinked to original sources

Single-cell-resolved natural giant virus infections reveal conserved protist immunity

Single-cell eukaryotes (protists) are key players in microbial ecosystems. Yet, our understanding of how they interact with viruses in nature and how antiviral defenses shape these relationships remains limited. Using a single-cell multi-omics approach, we mapped associations between giant viruses and their hosts and identified active giant-virus infections in an alpine lake protist community. In naturally infected dinoflagellates, infection was accompanied by the selective induction of viperin, an ancient antiviral enzyme conserved from bacteria to humans. We also observed virus-encoded homologs of immunity-related genes whose expression correlated with viperin expression, raising the possibility of a role in viral counter-defense. These findings reveal an ecological dimension of protist immunity and provide a framework for tracing the host-virus arms race across divergent cellular lineages.

microbiology↗

Giant endogenous viral elements in the genome of the model protist Euglena gracilis reveal past interactions with giant viruses

Giant viruses in the phylum Nucleocytoviricota have increasingly been found integrated into the genomes of diverse eukaryotes. Here we report 8 Giant Endogenous Viral Elements (GEVEs) in the genome of the microalgae Euglena gracilis. The GEVEs bear signatures of genomic erosion, including invasion of transposable elements and duplications, suggesting that they are incapable of reactivation and virion production. Most of the GEVEs exhibit high average amino acid identity and cluster near each other in phylogenies of viral marker genes, suggesting that they are derived from the same initial viral lineage. Phylogenetic analysis of nucleocytovirus marker proteins reveals the viruses belong to the order Asfuvirales in the same broader lineage that includes African swine fever virus (ASFV), abalone asfarvirus (AbalV), and GEVEs recently found in the fungus Rhizophagus irregularis and the marine gastropod Elysia marginata, suggesting that widespread host range transitions have occurred in this lineage. This work expands the diversity of known endogenous giant viruses and expands the host range of the Asfuvirales to include the superkingdom Discoba.

bioinformatics↗

Latent infection of an active giant endogenous virus in a unicellular green alga

Latency is a common strategy in a wide range of viral lineages, but its prevalence in giant viruses remains unknown. Here we describe the activity and viral production from a 617 kbp integrated giant viral element in the model green alga Chlamydomonas reinhardtii. We resolve the integrated viral region using long-read sequencing and show that viral particles are produced and released in otherwise healthy cultures. A diverse array of viral-encoded selfish genetic elements are expressed during GEVE reactivation and produce proteins that are packaged in virions. In addition, we show that field isolates of Chlamydomonas sp. harbor latent giant viruses related to the C. reinhardtii GEVE that exhibit similar infection dynamics, demonstrating that giant virus latency is prevalent in natural host communities. Our work reports the largest temperate virus documented to date and the first active GEVE identified in a unicellular eukaryote, substantially expanding the known limits of viral latency.

microbiology↗

The Microbiota of Moon Snail Egg Collars is Shaped by Host-Specific Factors

Moon Snails lay eggs using a mixture of mucus and sediment to form an egg mass commonly referred to as an egg collar. These collars do not appear to experience micro-biofouling or predation and this observation led us to hypothesize that the egg collars possess a chemically-rich microbiota that protect the egg collars from pathogens. Herein, we sought to gain an understanding of the bacterial composition of the egg collars by amplifying and sequencing the 16S rRNA gene from egg collar and sediment samples collected at four distinct geographical regions in SW Florida. Relative abundance and non-metric multidimensional scaling plots revealed distinct differences in the bacterial composition between the egg collar and sediment samples. In addition, the egg collars had a lower -diversity than the sediment, with specific genera being significantly enriched in the egg collars. Analysis of microorganisms consistent across two seasons suggests that Flavobacteriaceae make up a large portion of the core microbiota (36 - 58% of 16S sequences). We also investigated the natural product potential of the egg collar microbiota by sequencing a core biosynthetic gene, the adenylation domains (AD), within the gene clusters of non-ribosomal peptide synthetase (NRPS). AD sequences matched multiple modules within known bioactive NRPs biosynthetic gene clusters, suggesting production is possible within the egg collar system and lays the foundation for future studies into the chemical and ecological role of this microbiota. IMPORTANCEAnimals commonly partner with microorganisms to accomplish essential tasks, including chemically defending the animal host from predation and/or infections. Understanding animal-microbe partnerships and the molecules used by the microbe to defend the animals from pathogens or predation have the potential to lead to new pharmaceutical agents. However, very few of these systems have been investigated. A particularly interesting system are nutrient rich marine egg collars, which often lack visible protections, and are hypothesized to harbor beneficial microbes that protect the eggs. In this study, we gained an understanding of the bacterial strains that form the core microbiota of Moon Snail egg collars and gained a preliminary understanding of their natural product potential. This work lays the foundation for future work to understand the ecological role of the core microbiome and to study the molecules involved in chemically defending the Moon Snail eggs.

bioinformatics↗

Chimeric Origin of Eukaryotes from Asgard Archaea and Ancestral Giant Viruses

The details surrounding the evolution of complex cells remain some of the most enduring mysteries in biology. Recent evidence has demonstrated that Asgard archaea are the closest cellular relatives of eukaryotes, but several eukaryotic enzymes involved in key cellular processes lack phylogenetic affinity with archaea. In particular, phylogenies of eukaryotic DNA and RNA polymerases often support a 3-domain topology that is not consistent with an archaeal origin. Here we present comprehensive phylogenetic analysis of eukaryotic family B DNA polymerases and multimeric RNA polymerases and show that these core subunits of these enzymes are derived from the ancestors of modern giant viruses (phylum Nucleocytoviricota). Specifically, we show that the eukaryotic delta polymerase (Pol{delta}), a key processive polymerase required for genome replication in all eukaryotes, clusters within an ancient viral clade, strongly supporting a viral origin. By contrast, the other eukaryotic processive polymerase (Pol{varepsilon}), clusters within an Asgard archaeal clade. Together, these observations provide a strong and direct link between early eukaryotes, Asgard archaea, and giant viruses. Lastly, we provide a comprehensive phylogenetic analysis of eukaryotic multimeric RNA polymerases to confirm that RNA polymerase II, which is responsible for mRNA transcription in eukaryotes, is also derived from the ancestors of modern giant viruses. In total, our results support a model of eukaryogenesis in which complex cells emerged from a genomic chimera of Asgard archaea and an ancient viral lineage.

evolutionary biology↗

Polinton-like Viruses Associated with Entomopoxviruses Provide Insight into Replicon Evolution

Polinton-like viruses (PLVs) are a diverse group of small integrative dsDNA viruses that infect diverse eukaryotic hosts. Many PLVs are hypothesized to parasitize viruses in the phylum Nucleocytoviricota for their own propagation and spread. Here we analyze the genomes of novel PLVs associated with the occlusion bodies of entomopoxvirus (EV) infections of two separate lepidopteran hosts. The presence of these elements within EV occlusion bodies suggests that they are the first known hyperparasites of poxviruses. We find that these PLVs belong to two distinct lineages that are highly diverged from known PLVs. These PLVs possess mosaic genomes, and some essential genes share homology with mobile genes within EVs. Based on this homology and observed PLV mosaicism, we propose a mechanism to explain the turnover of PLV replication and integration genes.

genomics↗

Resolving ancient gene transfers clarifies the early co-evolution of eukaryotes and giant viruses

Members of the phylum Nucleocytoviricota, also called "giant viruses" due to their large physical dimensions and genome lengths, are a diverse group of dsDNA viruses that infect a wide range of eukaryotic hosts. Nucleocytoviruses likely evolved from smaller viruses, but the timing of their emergence and its relationship to the early evolution of eukaryotes remains unclear. Recent work has shown that the genomes of nucleocytoviruses often encode Eukaryotic Signature Proteins (ESPs) - including histones, vesicular trafficking factors, cytoskeletal components, and elements of RNA and DNA processing - that occur only rarely outside of eukaryotes. To investigate patterns of gene exchange between viruses and eukaryotes and possibly shed light on the early evolution of both, we examined the occurrence of viral-encoded ESPs (vESPs) and performed a comprehensive phylogenetic reconstruction on a subset that are widespread in nucleocytoviruses. Our results demonstrate that vESPs involved in cytoskeletal structure, ubiquitin system, and vesicular trafficking were acquired multiple times independently by nucleocytoviruses at different timepoints after the emergence of the eukaryotic supergroups. In contrast, vESPs involved in DNA and RNA processing are placed deep in their respective phylogenies, indicative of ancient gene exchange between nucleocytoviruses and eukaryotes. Examination of vESPs that could be rooted in archaea revealed that nucleocytoviruses likely acquired some of these genes prior to the emergence of the last eukaryotic common ancestor (LECA). Importantly, our findings also suggest that the eukaryotic delta DNA polymerase was acquired from nucleocytoviruses sometime during eukaryogenesis, underscoring the importance of viruses for early eukaryotic evolution. Collectively, these results suggest that gene exchange between nucleocytoviruses and eukaryotes played important roles in the evolution of both prior to the emergence of LECA.

evolutionary biology↗

Homing in on the rare virosphere reveals the native host of giant viruses

Giant viruses (phylum Nucleocytoviricota) are globally distributed in aquatic ecosystems1,2. They play major roles as evolutionary drivers of eukaryotic plankton3 and regulators of global biogeochemical cycles4. Recent metagenomic studies have significantly expanded the known diversity of marine giant viruses1,5-7, but we still lack fundamental knowledge about their native hosts, thereby hindering our understanding of their lifecycle and ecological importance. Here, we aim to discover the native hosts of giant viruses using a novel, sensitive single-cell metatranscriptomic approach. By applying this approach to natural plankton communities, we unraveled an active viral infection of several giant viruses, from multiple lineages, and identified their native hosts. We identify a rare lineage of giant virus (Imitervirales-07) infecting a minute population of protists (class Katablepharidaceae) and revealed the prevalence of highly expressed viral-encoded cell-fate regulation genes in infected cells. Further examination of this host-virus dynamics in a temporal resolution suggested this giant virus controls its host population demise. Our results demonstrate how single-cell metatranscriptomics is a sensitive approach for pairing viruses with their authentic hosts and studying their ecological significance in a culture-independent manner in the marine environment.

microbiology↗

Contrasting drivers of abundant phage and prokaryotic communities in tropical, coastal ecosystems across the Isthmus of Panama

Phages, or viruses that infect bacteria and archaea, are ubiquitous and abundant members of Earths ecosystems that impact the flow of nutrients, evolution of microbes, and food web dynamics by selectively infecting and killing their prokaryotic hosts. Because phages can only replicate through their hosts, they are inherently linked to processes impacting their hosts distribution and susceptibility to infection. Despite these links, phages can also be affected by environmental parameters independent of their hosts, such as pH or salinity which impact cell adsorption or virion degradation. To understand these complex links, in this study, we leverage the unique ecological context of the Isthmus of Panama, which narrowly disconnects the productive Tropical Eastern Pacific (TEP) and Tropical Western Atlantic (TWA) provinces and compare factors that shape active marine phage and prokaryotic communities. Metagenomic sequencing of seawater from mangroves and reefs of both the TEP and TWA coasts of Panama suggest that pronounced environmental gradients, such as along the TEP mangrove rivers, result in common dispersal and physicochemical parameters shaping both prokaryotic and phage community composition and diversity. Conversely, we find that when environmental conditions are relatively similar across adjacent habitats, such as between the mangroves and reefs in the TWA, prokaryotic communities are more influenced by local abiotic conditions while phage communities are shaped more by dispersal. Collectively, this work provides a framework for addressing the co-variability between viruses and their hosts in marine systems and for identifying the different factors that drive consistent versus disparate trends in community shifts, which is essential to inform models of these interactions in biogeochemical cycling.

microbiology↗

A Timeline of Bacterial and Archaeal Diversification in the Ocean

Microbial plankton play a central role in marine biogeochemical cycles, but the timing in which abundant lineages diversified into ocean environments remains unclear. Here, we reconstructed the timeline in which major clades of bacteria and archaea colonized the ocean using a high-resolution benchmarked phylogenetic tree that allows for simultaneous and direct comparison of the ages of multiple divergent lineages. Our findings show that the diversification of the most prevalent marine clades spans throughout a period of 2.2 Ga, with most clades colonizing the ocean during the last 800 million years. The oldest clades - SAR202, SAR324, Ca. Marinimicrobia, and Marine Group II - diversified around the time of the Great Oxidation Event (GOE), during which oxygen concentration increased but remained at microaerophilic levels throughout the Mid-Proterozoic, consistent with the prevalence of some clades within these groups in oxygen minimum zones today. We found the diversification of the prevalent heterotrophic marine clades SAR11, SAR116, SAR92, SAR86, and Roseobacter as well as the Marine Group I, to occur near to the Neoproterozoic Oxygenation Event (0.8-0.4 Ga). The diversification of these clades is concomitant with an overall increase of oxygen and nutrients in the ocean at this time, as well as the diversification of eukaryotic algae, consistent with the previous hypothesis that the diversification of heterotrophic bacteria is linked to the emergence of large eukaryotic phytoplankton. The youngest clades correspond to the widespread phototrophic clades Prochlorococcus, Synechococcus, and Crocosphaera, whose diversification happened after the Phanerozoic Oxidation Event (0.45-0.4 Ga), in which oxygen concentrations had already reached their modern levels in the atmosphere and the ocean. Our work clarifies the timing at which abundant lineages of bacteria and archaea colonized the ocean, thereby providing key insights into the evolutionary history of lineages that comprise the majority of prokaryotic biomass in the modern ocean.

evolutionary biology↗

Infection strategy and biogeography distinguish cosmopolitan groups of marine jumbo bacteriophages

Recent research has underscored the immense diversity and key biogeochemical roles of large DNA viruses in the ocean. Although they are important constituents of marine ecosystems, it is often difficult to detect these viruses due to their large size and complex genomes. This is true for "jumbo" bacteriophages, which have genome sizes >200 kbp and large capsids reaching up to 0.45 m in diameter. In this study, we sought to assess the genomic diversity and distribution of these bacteriophages in the ocean by developing a bioinformatic pipeline to generate and validate jumbo phage genomes from metagenomes. We recover 85 marine jumbo phages that ranged in size from 201-498 kilobases, and we examine their genetic similarities and biogeography together with a reference database of marine jumbo phage genomes. By analyzing Tara Oceans metagenomic data we show that jumbo phages are less common in <0.22 m size fractions but are widespread in larger fractions, consistent with their large size. Our network-based analysis of gene sharing patterns reveals that jumbo bacteriophage belong to five genome clusters that are typified by diverse replication strategies, genomic repertoires, and potential host ranges. Our analysis of jumbo phage distributions in the ocean reveals that depth is a major factor shaping their biogeography, with some phage genome clusters exhibiting higher relative abundance in either surface or mesopelagic waters, respectively. Taken together, our findings demonstrate that jumbo phages are widespread community members in the ocean with complex genomic repertoires and ecological impacts that warrant further targeted investigation.

microbiology↗

Genome size distributions in bacteria and archaea are strongly linked to phylogeny

The evolutionary forces that determine genome size in bacteria and archaea have been the subject of intense debate over the last few decades. Although the preferential loss of genes observed in prokaryotes is explained through the deletional bias, factors promoting and preventing the fixation of such gene losses remain unclear. Moreover, statistical analyses on this topic have typically been limited to a narrow diversity of bacteria and archaea without considering the potential bias introduced by the shared recent ancestry of many lineages. In this study, we used a phylogenetic generalized least-squares (PGLS) analysis to evaluate the effect of different factors on the genome size of a broad diversity of bacteria and archaea. We used dN/dS to estimate the strength of purifying selection, and 16S copy number as a proxy for ecological strategy, which have both been postulated to play a role in shaping genome size. After model fit, Pagels lambda indicated a strong phylogenetic signal in genome size, suggesting that the diversification of this trait is strongly influenced by shared evolutionary histories. As a predictor variable, dN/dS showed a poor predictability and non-significance when phylogeny was considered, consistent with the view that genome reduction can occur under either weak or strong purifying selection depending on the ecological context. Copies of 16S rRNA showed poor predictability but maintained significance when accounting for non-independence in residuals, suggesting that ecological strategy as approximated from 16S rRNA copies might play a minor role in genome size variation. Altogether, our results indicate that genome size is a complex trait that is not driven by any singular underlying evolutionary force, but rather depends on lineage- and niche-specific factors that will vary widely across bacteria and archaea. Author SummaryThe evolutionary forces driving genome size in bacteria and archaea have been subject to debate during the last decades. Independent comparative analyses have suggested that unique variables, such as the strength of selection, environmental complexity, and mutation rate, are the main drivers of this trait, which complicates generalizations across the Tree of Life. Here, we applied a phylogeny-based statistical approach to assess how tightly genome size is linked to evolutionary history in bacteria and archaea. Moreover, we also evaluated the predictability of genome size from the strength of purifying selection and ecological strategy on a broad diversity of bacteria and archaea genomes. Our approach indicates that genome size in prokaryotes is strongly dependent on phylogenetic history, and that genome size is the result of the interaction of variables like past events, current selection regimes, and environmental complexity that are clade dependent.

evolutionary biology↗

High Transcriptional Activity and Diverse Functional Repertoires of Hundreds of Giant Viruses in a Coastal Marine System

Viruses belonging to the Nucleocytoviricota phylum are globally-distributed and include members with notably large genomes and complex functional repertoires. Recent studies have shown that these viruses are particularly diverse and abundant in marine systems, but the magnitude of actively replicating Nucleocytoviricota present in ocean habitats remains unclear. In this study, we compiled a curated database of 2,431 Nucleocytoviricota genomes and used it to examine the gene expression of these viruses in a 2.5-day metatranscriptomic time-series from surface waters of the California Current. We identified 145 viral genomes with high levels of gene expression, including 90 Imitervirales and 49 Algavirales viruses. In addition to recovering high expression of core genes involved in information processing that are commonly expressed during viral infection, we also identified transcripts of diverse viral metabolic genes from pathways such as glycolysis, the TCA cycle, and the pentose phosphate pathway, suggesting that virus-mediated reprogramming of central carbon metabolism is common in oceanic surface waters. Surprisingly, we also identified viral transcripts with homology to actin, myosin, and kinesin domains, suggesting that viruses may use them to manipulate host cytoskeletal dynamics during infection. We performed phylogenetic analysis on the virus-encoded myosin and kinesin proteins, which demonstrated that most belong to deep-branching viral clades, but that others appear to have been acquired from eukaryotes more recently. Our results highlight a remarkable diversity of active Nucleocytoviricota in a coastal marine system and underscore the complex functional repertoires expressed by these viruses during infection. ImportanceThe discovery of giant viruses has transformed our understanding of viral complexity. Although viruses have traditionally been viewed as filterable infectious agents that lack metabolism, giant viruses can reach sizes rivalling cellular lineages and possess genomes encoding central metabolic processes. Recent studies have shown that giant viruses are widespread in aquatic systems, but the activity of these viruses and the extent to which they reprogram host physiology in situ remains unclear. Here we show that numerous giant viruses consistently express central metabolic enzymes in a coastal marine system, including components of glycolysis, the TCA cycle, and other pathways involved in nutrient homeostasis. Moreover, we found expression of several viral-encoded actin, myosin, and kinesin genes, indicating viral manipulation of the host cytoskeleton during infection. Our study reveals a high activity of giant viruses in a coastal marine system and indicates they are a diverse and underappreciated component of microbial diversity in the ocean.

microbiology↗

Comparative Genomics and Environmental Distribution of Large dsDNA viruses in the family Asfarviridae

The Asfarviridae is a family of Nucleo-Cytoplasmic Large DNA Viruses (NCLDV) of which African swine fever virus (ASFV) is the most well-characterized. Recently the discovery of several Asfarviridae members other than ASFV has suggested that this family represents a diverse and cosmopolitan group of viruses, but the genomics and distribution of this family have not been studied in detail. To this end we analyzed five complete genomes and 35 metagenome-assembled genomes (MAGs) of viruses from this family to shed light on their evolutionary relationships and environmental distribution. The Asfarvirus MAGs derive from diverse marine, freshwater, and terrestrial habitats, underscoring the broad environmental distribution of this family. We present phylogenetic analyses using conserved marker genes and whole-genome comparison of pairwise average amino acid identity values, revealing a high level of genomic divergence across disparate Asfarviruses. Further, we found that Asfarviridae genomes encode genes with diverse predicted metabolic roles and detectable sequence homology to proteins in bacteria, archaea, and different eukaryotes, highlighting the genomic chimerism that is a salient feature of NCLDV. Our read mapping from Tara oceans metagenomic data also revealed that three Asfarviridae MAGs were present in multiple marine samples, indicating that they are widespread in the ocean. In one of these MAGs we identified four marker genes with >95% amino acid identity to genes sequenced from a virus that infects the dinoflagellate Heterocapsa circularisquama (HcDNAV). This suggests a potential host for this MAG, which would thereby represent a near-complete genome of a dinoflagellate-infecting giant virus. Together, these results show that Asfarviridae are ubiquitous, comprise similar sequence divergence as other NCLDV families, and include several members that are widespread in the ocean and potentially infect ecologically important protists.

microbiology↗

Dominant Remodeling of Cattle Rumen Microbiome by Schedonorus arundinaceus (Tall Fescue) KY-31 Carrying a Fungal Endophyte

Tall fescue KY-31 feeds ~20% of the beef cattle in the United States. It carries a fungal endophyte that produces ergovaline, which causes toxicosis in cattle, leading to $2 billion revenue loss annually. The MaxQ cultivar of the grass is non-toxic, but less attractive economically. To develop ways of mitigating the toxicity, the rumen microbiome of cattle consuming KY-31 and MaxQ have been analyzed, principally for identifying ergovaline transforming microorganisms and often using fecal microbiome as a surrogate. We have hypothesized that KY-31 not only causes toxicosis, but also impacts rumen metabolism broadly, and tested the hypothesis by analyzing rumen microbiome compositions of cattle that grazed MaxQ with an intervening KY-31 grazing period with 16S rRNA-V4 element as identifier. We found that KY-31 remodeled the cellulolytic and saccharolytic communities substantially. This effect was not evident at whole microbiome levels but in the compositions of sessile and planktonic fractions. A move from MaxQ to KY-31 lowered the Firmicutes abundance in the sessile fraction and increased it in planktonic part and caused an opposite effect for Bacteroidetes, although the total abundances of these dominant rumen organisms remained unchanged. In the sessile fraction, the abundances of Fibrobacter, which degrades less degradable fibers, and certain cellulolytic Firmicutes such as Pseudobutyrivibrio and Butyrivibrio 2, dropped, and these losses were apparently compensated by increased occurrences of Eubacterium and specific Ruminococcaceae and Lachnospiraceae. In planktonic fraction the Tenericutes abundance increased as saccharolytic Bacteroidetes level dropped. Several potential ergovaline degraders were enriched. A return to MaxQ restored the original Firmicutes and Bacteroidetes distributions. However, the Fibrobacter and Butyrivibrio 2 abundances remained low and their substitutes maintained significant presence. The rumen microbiome was influenced minimally by animals fescue toxicosis and was distinct from previously reported fecal microbiomes in composition. In summary, KY-31 and MaxQ cultivars of tall fescue were digested in the cattle rumen with distinct consortia and the KY-31-specific features were dominant. The study highlighted the importance of analyzing sessile and planktonic fractions separately.

microbiology↗

ViralRecall: A Flexible Command-Line Tool for the Detection of Giant Virus Signatures in Omic Data

Giant viruses are widespread in the biosphere and play important roles in biogeochemical cycling and host genome evolution. Also known as Nucleo-Cytoplasmic Large DNA Viruses (NCLDV), these eukaryotic viruses harbor the largest and most complex viral genomes known. Recent studies have shown that NCLDV are frequently abundant in metagenomic datasets, and that sequences derived from these viruses can also be found endogenized in diverse eukaryotic genomes. The accurate detection of sequences derived from NCLDV is therefore of great importance, but this task is challenging owing to both the high level of sequence divergence between NCLDV families and the extraordinarily high diversity of genes encoded in their genomes, including some encoding for metabolic or translation-related functions that are typically found only in cellular lineages. Here we present ViralRecall, a bioinformatic tool for the identification of NCLDV signatures in omic data. This tool leverages a library of Giant Virus Orthologous Groups (GVOGs) to identify sequences that bear signatures of NCLDV. We demonstrate that this tool can effectively identify NCLDV sequences with high sensitivity and specificity. Moreover, we show that it can be useful both for removing contaminating sequences in metagenome-assembled viral genomes as well as the identification of eukaryotic genomic loci that derived from NCLDV. ViralRecall is written in Python 3.5 and is freely available on GitHub: https://github.com/faylward/viralrecall.

bioinformatics↗

Community-scale Synchronization and Temporal Partitioning of Gene Expression, Metabolism, and Lipid Biosynthesis in Oligotrophic Ocean Surface Waters

Sunlight drives daily rhythms of photosynthesis, growth, and division of photoautotrophs throughout the surface oceans. However, the cascading impacts of oscillatory light input on diverse microbial communities and community-scale metabolism remains unclear. Here we use an unsupervised machine learning approach to show that a small number of diel archetypes can explain pervasive periodic dynamics amongst more than 65,000 distinct time series, including transcriptional activity, macromolecules, lipids, and metabolites from the North Pacific Subtropical Gyre. Overall, we find evidence for synchronous timing of carbon-cycle gene expression that underlie daily oscillations in the concentrations of particulate organic carbon. In contrast, we find evidence of asynchronous timing in gene transcription related to nitrogen metabolism and related metabolic processes consistent with temporal niche partitioning amongst microorganisms in the bacterial and eukaryotic domains.

ecology↗

Diel Oscillations of Particulate Metabolites Reflect Synchronized Microbial Activity in the North Pacific Subtropical Gyre

Light is the primary input of energy into the sunlit ocean, driving daily oscillations in metabolism of primary producers. The consequences of this solar forcing have implications for the whole microbial community, yet in situ measurements of metabolites, direct products of cellular activity, over the diel cycle are scarce. We evaluated community-level biochemical consequences of diel oscillations in the North Pacific Subtropical Gyre by quantifying 79 metabolites in particulate organic matter in surface waters every four hours over eight days. Total particulate metabolite concentration peaked at dusk, even when normalized to biomass estimates. The concentrations of 70% of individual metabolites exhibited 24-hour periodicity. Despite the diverse organisms that use them, primary metabolites involved in anabolic processes and redox maintenance had significant 24-hour periodicity. Osmolytes exhibited the largest diel oscillations, implying rapid turnover and metabolic roles beyond cell turgor maintenance. Metatranscriptome analysis revealed the taxa involved in production and consumption of some metabolites, including the osmolyte trehalose. This compound displayed the largest diel oscillations in abundance and was likely produced by the nitrogen-fixing cyanobacterium Crocosphaera for energy storage. These findings demonstrate that paired measurements of particulate metabolites and transcripts resolve strategies microbes use to manage daily energy and redox oscillations.

ecology↗