Biology subjects

Weinheimer, A. R.

Publications and source records attributed to Weinheimer, A. R..

6 recordsLinked to original sources

bioRxiv2026

Global, single-cell-resolution of antiviral defenses in marine prokaryoplankton

Background Growing evidence suggests that variation in resistance to viral infections by marine prokaryoplankton enables the coexistence of both viral and host populations. Recent experimental work on model organisms has revealed dozens of novel antiviral defense mechanisms. This diversity has prompted the hypothesis of the pan-immunity model, in which diverse defenses are a shared resource among closely related individuals to broaden the population's resistance and minimize an individual's burden. The composition and abundance of such defense pools in natural microbial communities, however, remain largely unknown. Here, we begin to parameterize resistance in marine prokaryotes and define their defense repertoire by quantifying antiviral defenses across thousands of randomized single-amplified genomes (SAGs) from a global collection of seawater samples. Results Prokaryoplankton SAGs contained an average of 1.1 defenses, with dark ocean (200 m - 11 km) prokaryotes having a slightly higher genomic load of defenses as compared to the sunlit, surface ocean. The number of defenses per cell was taxon-specific, with little or no relationship to depth, taxon abundance, estimated maximal growth rate, or viral infection rate. The most numerous and taxonomically widespread defenses were restriction modification systems, followed by dGTPase (mostly in Pelagibacterales) in the sunlit ocean and AbiU (mostly in Nitrososphaerales) in the dark ocean. Most other defense types were rare (< 0.1% SAGs) yet distributed across distant taxa (> 3 phyla). We found evidence for the cross-domain exchange of the most common defense system, RM II, between archaea and bacteria, which improves our understanding of the biology of this prevalent defense and could be consequential in predicting target motifs for connecting viruses with potential hosts in epigenetic studies. Conclusions Collectively, these results suggest lineages restrict genomic real estate for defenses yet enable extensive lateral transfer, potentially for the maintenance of defense variation at the community level rather than only among closely related individuals. This study provides a quantitative atlas of prokaryoplankton immunity toward grounding our understanding of virus-microbe interactions in the Earth's largest biome, the open ocean.

microbiology↗

bioRxiv2026

Single-cell-resolved frequency and modes of phage interactions with prokaryoplankton in the tropical surface ocean

Marine planktonic viruses play critical roles in shaping microbial communities and driving global biogeochemical cycles. However, quantitative, microbiome-wide analyses of marine prokaryoplankton-virus interactions in situ and their ecological impacts remain challenging due to the vast diversity of viral genomes and interaction modes and the limitations of existing methodologies. Here, we utilized GORG-Tropics, a global collection of 12,715 single amplified genomes (SAGs) generated from randomly sampled marine prokaryoplankton cells, to determine the frequency and modes of their interactions with viruses in the tropical surface ocean. We found 4.2% (range 1%-19% among samples) of GORG-Tropics SAGs to contain phage genomic material, with the highest frequency found in productive ocean regions. Prokaryoplankton lineages known to have high metabolic rates, including Prochlorococcus and Rhodobacterales, had a substantially larger fraction of cells associated with viruses (10-12% of SAGs) as compared to the less active but highly abundant lineages including Pelagibacterales (2.2% of SAGs). Cell-virus associations indicative of lysogeny were elevated in Alphaproteobacteria relative to other taxa. The collection of phages recovered from individual SAGs exhibited genomic diversity that bridged order-level taxonomies, indicating high diversity and genomic connectivity within wild phage populations. A substantial fraction of the observed cell-virus associations disagreed with the computationally predicted host identity of the virus, indicative of non-infective interactions. The extent of genetic exchange across tailed bacteriophages infecting different hosts, and connected to taxonomically distant phages provided further evidence for the role of non-infective phage entry in the lateral transfer between tailed phages. This study provides large-scale quantitative evidence of viral infection rates in the collective prokaryoplankton community across the global surface tropical ocean through large-scale identification and quantification of the specific phages, hosts, and modes of interaction at the resolution of individual cells. Our results confirm prior reports on the overall frequency of prokaryoplankton infections with viruses in the oligotrophic tropical surface ocean. Our findings uncover non-infective phage-cell associations that may be contributing to the lateral transfer of viral genes and the nutrition of marine prokaryoplankton.

microbiology↗

bioRxiv2024

Towards a unifying phylogenomic framework for tailed phages

BackgroundClassifying viruses systematically has remained a key challenge of virology due to the absence of universal genes and vast genetic diversity of viruses. In particular, the most dominant and diverse group of viruses, the tailed double-stranded DNA viruses of prokaryotes belonging to the class Caudoviricetes, lack sufficient homology in the genetic machinery that unifies them to reconstruct inclusive, stable phylogenies of these genes. While previous approaches to organize tailed phage diversity have managed to distinguish various taxonomic levels, these methods are limited in scalability and reproducibility, and they do not include modes of evolution, like gene gains and losses. ResultsHere, we present a novel, comprehensive and reproducible framework for examining evolutionary relationships of tailed phages. In this framework, we compare phage genomes based on presences and absences of a fixed set of gene families which is used as binary trait data that is input into maximum likelihood models, which include heterogeneous rates of trait losses and gains. Our resulting phylogeny stably recovers known taxonomic families of tailed phages, with and without the inclusion of metagenomic phages. We also quantify the mosaicism of replication and structural genes among known families. Our results suggest that these exchanges likely underpin the emergence of new families. Additionally, we apply this framework to large phages (>100 kilobases) to map emergences of traits associated with genome expansion. ConclusionTaken together, this evolutionary framework for charting and organizing tailed phage diversity improves the systemization of phage taxonomy, which can unify phage studies and advance our understanding of their evolution.

genomics↗

bioRxiv2023

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↗

bioRxiv2022

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↗

bioRxiv2019

Dynamic Genome Evolution and Blueprint of Complex Virocell Metabolism in Globally-Distributed Giant Viruses

The discovery of giant viruses with large genomes has transformed our understanding of the limits of viral complexity in the biosphere, and subsequent research in model virus-host systems has advanced our knowledge of intricate mechanisms used by these viruses to take over host cells during infection. The extent of the metabolic diversity encoded by these viruses in the environment is less well-understood, however, and their potential impact on global biogeochemical cycles remains unclear. To address this, we generated 501 metagenome-assembled genomes (MAGs) of NCLDVs from diverse environments around the globe and analyzed their encoded functional diversity and potential for reprogramming host physiology. We found that 476 (95%) of the MAGs belonged to the Mimiviridae and Phycodnaviridae families, and of these we recovered 96% from aquatic environments, highlighting the diversity of these viral families in global freshwater and marine systems. MAGs encoded diverse genes predicted to be involved in nutrient uptake and processing, light harvesting, central nitrogen metabolism, and the manipulation of cell death, underscoring the complex interplay between these viruses and their hosts. Surprisingly, numerous genomes encoded genes involved in glycolysis, gluconeogenesis, and the TCA cycle, including one genome with a 70%-complete glycolytic pathway, suggesting that many of these viruses can even reprogram fundamental aspects of their hosts central carbon metabolism. Phylogenetic trees of NCLDV metabolic genes together with their cellular homologs revealed distinct clustering of viral sequences into divergent clades, indicating these metabolic genes are virus-specific and were acquired in the distant past. Our findings reveal that diverse NCLDV genomes encode complex, cell-like metabolic capabilities with evolutionary histories that are largely independent of cellular life, strongly implicating them as distinct drivers of biogeochemical cycles in their own right.

microbiology↗