Virus-Host Infection Dynamics of Marine Single-Celled Eukaryotes Resolved from Metatranscriptomics

Abstract

microbiology 21 22 23 24 25 26 2 | M o n i r u z z a m a n e t a l .Abstract 27Metatranscriptomics has emerged as a tool in microbial ecology that can resolve the functional 28 landscape of both prokaryotes and eukaryotes within a community. In this study, we extend the 29 potential of metatranscriptomics to probe active virus infections and virus-host relationships in 30 marine systems. Polyadenylation-selected RNA-seq data were examined from microbial 31 communities in two productive marine environments: a brown tide bloom event dominated by 32Aureococcus anophagefferens in Quantuck Bay, NY, and a diatom-dominated plankton 33 community in Narragansett Bay, RI. Active infections by diverse giant viruses (NCLDVs) of 34 algal and non-algal hosts were found at both sites. Ongoing infections of A. anophagefferens by 35 a known Mimiviridae (AaV) were observed during both the peak and decline of the bloom. 36Bloom decline was also accompanied by increased activity for viruses other than AaV, including 37 (+) ssRNA viruses. In Narragansett Bay, increased temporal reso′lution revealed active NCLDVs 38 with both 'boom-and-bust' as well as 'steady-state infection'-like ecologies. Statistical co-39 occurrence examinations of the dsDNA, ssRNA and dsRNA markers within the data revealed a 40 broad spectrum of statistically strong and significant virus-host relationships that included both 41 known as well as novel interactions. Our approach offers a method for screening the diversity 42 and dynamics of active viral infections in natural systems and develops links between viruses 43 and their potential hosts in situ. 44 45 3 | M o n i r u z z a m a n e t a l . Significance 46Viruses are important partners in ecosystem scale ecology, yet their study to date is primarily 47 limited to single virus-host infection models in the laboratory or limited to "potential-actions" 48 derived from metagenomics analyses. Using metatranscriptomic sequences from polyadenylated-49 RNA selected samples, we have simultaneously captured information regarding eukaryotic 50 diversity and active infection by viruses with dsDNA genomes, resulting in a statistical 51 opportunity to predict "who is infecting whom". This approach further provides concurrent 52 insight regarding viruses with ssRNA and dsRNA genomes, capturing dynamics for the 53 communities of viruses infecting single-celled eukaryotes. Given the central role of these 54 plankton in global scale processes, our efforts result in a transformational step-forward regarding 55 the study of in situ virus-host interactions. 56 57

Virome Variation during Sea Star Wasting Disease Progression in Pisaster ochraceus (Asteroidea, Echinodermata)

“…Furthermore, contigs clustered with iflaviruses ( Iflaviridae ; contig 91247) and marnaviruses ( Marnaviridae ; contig 12092) by phylogenetic analyses ( Figure 4 ). Picornavirus-like genome fragments mostly matched viral genomes recovered from transcriptomic surveys of marine invertebrates (mollusks and crustacea) [ 22 , 41 ] and picoeukaryotes [ 42 ]. Picornaviruses have been previously recovered from asteroids [ 2 , 5 ] and holothurians [ 17 ].…”

“…Picornaviruses have been previously recovered from asteroids [ 2 , 5 ] and holothurians [ 17 ]. Since several genome fragments recovered in this survey matched most closely picornaviruses recovered from protists [ 42 ], it is possible that they were associated with protozoa associated with wasting tissues. Previous work has revealed the presence of presumably fungal viruses and a wide richness of protistan rRNAs in metagenomes prepared from material purified from <0.2 µm filtered tissue homogenates [ 17 ].…”

Virome Temporal Variation During Sea Star Wasting Disease Progression in Pisaster ochraceus (Asteroidea, Echinodermata)

“…Picornaviruses have been previously recovered from asteroids [2,5] and holothurians [17]. Since several genome fragments recovered in this survey matched most closely picornaviruses recovered from protists [41], it is possible that they were associated with protozoa associated with wasting tissues. Previous work has revealed the presence of presumably fungal viruses and a wide richness of protistan rRNAs in metagenomes prepared from material purified from < 0.2 µm filtered tissue homogenates [17].…”

“…4). Picornavirus-like genome fragments mostly matched viral genomes recovered from transcriptomic surveys of marine invertebrates (mollusks and crustacea) [21,40] and picoeukaryotes [41]. Picornaviruses have been previously recovered from asteroids [2,5] and holothurians [17].…”

A Student’s Guide to Giant Viruses Infecting Small Eukaryotes: From Acanthamoeba to Zooxanthellae

“…Building on the above, it is clear from a survey of the literature that researchers identified candidate protist-giant virus systems well before Mimivirus was documented (Table 3). In the late 1960s and early 1970s, the expanded availability of transmission electron microscopes to researchers resulted in a series of observations concerning the presence of large virus-like particles inside algal cells [107,109]. In many cases, these virus–host systems have been largely ignored by the scientific community, creating a broad spectrum of opportunities for researchers to begin to cultivate these plankton in an effort to isolate and characterize new giant viruses.…”