Virologs, viral mimicry, and virocell metabolism: the expanding scale of cellular functions encoded in the complex genomes of giant viruses

Moniruzzaman, Mohammad; Erazo Garcia, Maria Paula; Farzad, Roxanna; Ha, Anh D; Jivaji, Abdeali; Karki, Sangita; Sheyn, Uri; Stanton, Joshua; Minch, Benjamin; Stephens, Danae; Hancks, Dustin C; Rodrigues, Rodrigo A L; Abrahao, Jonatas S; Vardi, Assaf; Aylward, Frank O

doi:10.1093/femsre/fuad053

Cited by 11 publications

(5 citation statements)

References 268 publications

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“…Viruses from the phylum Nucleocytoviricota (NCLDV), also known as giant viruses, are abundant in the Earth’s oceans and have been found to inhabit a range of different environments as well as modulate host metabolism and genome evolution (41,42). The main hosts for these viruses include microeukaryotes such as unicellular algae and protists.…”

Section: Resultsmentioning

confidence: 99%

Active prokaryotic and eukaryotic viral ecology across spatial scale in a deep-sea brine pool

Minch,

Chakraborty,

Purkis

et al. 2024

Preprint

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Deep-sea brine pools represent rare, extreme environments that focus biodiversity at bathyal to abyssal depths. Despite their small size and distribution, brine pools represent important ecosystems to study because they provide unique insight into the limits of life on Earth, and by analogy, the plausibility of life beyond it. A distinguishing feature of many brine pools is the presence of thick benthic microbial mats which develop at the brine-seawater interface. While these bacterial and archaeal communities have received moderate attention, little is known about the viral communities and their interactions with host populations in these environments. To bridge this knowledge gap, we leveraged metagenomic and metatranscriptomic data from three distinct zones within the NEOM brine pool system (Gulf of Aqaba) to gain insights into the active viral ecology around the pools. Here, we report a remarkable diversity and activity of viruses of all nucleic acid types and genome sizes that infect prokaryotic and eukaryotic hosts in this environment. These include giant viruses (phylum: Nucleocytoviricota), RNA viruses, jumbo phages, and polinton-like viruses (PLVs). Many of these appeared to form distinct clades showing the possibility of untapped viral diversity in the brine pool ecosystem. Zone-specific differences in viral community composition and infection strategy were also observed with lysogenic phages seeming to dominate the bacterial mat further away from the pools center. Through host matching, viruses infecting metabolically important bacteria and archaea were observed - including a linkage between a jumbo phage and a key manganese-oxidizing and arsenic-metabolizing bacterium. Our findings shed light on the role of viruses in modulating the brine pool microbial community dynamics and biogeochemistry through revealing novel viral diversity, host-virus associations, and spatial-scale heterogeneity in viral dynamics in these extreme environments. These results will provide crucial foundation for further investigation into the adaptations of viruses and their microbial hosts in extreme habitats in the marine ecosystem.

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Section: Resultsmentioning

confidence: 99%

Active prokaryotic and eukaryotic viral ecology across spatial scale in a deep-sea brine pool

Minch,

Chakraborty,

Purkis

et al. 2024

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…Viruses from the phylum NCLDV, are abundant in the Earth’s oceans and have been found to inhabit a range of different environments as well as modulate host metabolism and genome evolution [ 83 , 84 ]. The main hosts for these viruses include microeukaryotes such as unicellular algae and protists.…”

Section: Resultsmentioning

confidence: 99%

Active prokaryotic and eukaryotic viral ecology across spatial scale in a deep-sea brine pool

Minch,

Chakraborty,

Purkis

et al. 2024

ISME Communications

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Deep-sea brine pools represent rare, extreme environments, providing unique insight into the limits of life on Earth, and by analogy, the plausibility of life beyond it. A distinguishing feature of many brine pools is presence of thick microbial mats which develop at the brine-seawater interface. While these bacterial and archaeal communities have received moderate attention, viruses and their host interactions in these environments remain underexplored. To bridge this knowledge gap, we leveraged metagenomic and metatranscriptomic data from three distinct zones within the NEOM brine pool system (Gulf of Aqaba) to reveal the active viral ecology around the pools. We report a remarkable diversity and activity of viruses infecting microbial hosts in this environment, including giant viruses, RNA viruses, jumbo phages, and polinton-like viruses. Many of these form distinct clades – suggesting presence of untapped viral diversity in this ecosystem. Brine pool viral communities exhibit zone-specific differences in infection strategy - with lysogeny dominating the bacterial mat further away from the pool’s center. We linked viruses to metabolically important prokaryotes - including association between a jumbo phage and a key manganese-oxidizing and arsenic-metabolizing bacterium. These foundational results illuminate the role of viruses in modulating brine pool microbial communities and biogeochemistry through revealing novel viral diversity, host associations, and spatial heterogeneity in viral dynamics.

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“…Mitochondria are also important antiviral responders in host immunity and are exposed to unique in vivo environments, which were demonstrated by increasing evidence [ 25 ]. Due to the important roles that mitochondria play against viral infections, viruses also change to adapt themselves better in vivo , by generating large populations of viral genome-encoded virologs [ 50 ], which include mimicking the host's enzymes and interfering with the mitochondrial tricarboxylic acid (TCA) cycle and ETC reaction of host cells to inhibit the apoptosis of infected cells. The presence of virologs will further increase viral persistence and the stress and vulnerability of the mitochondria during viral infections [ 24 , 25 ].…”

Section: Discussionmentioning

confidence: 99%

Mitochondrial DNA Missense Mutations ChrMT: 8981A > G and ChrMT: 6268C > T Identified in a Caucasian Female with Myalgic Encephalomyelitis/Chronic Fatigue Syndrome (ME/CFS) Triggered by the Epstein–Barr Virus

Tang-Siegel,

Maughan,

Frownfelter

et al. 2024

Case Reports in Genetics

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Myalgic encephalomyelitis/chronic fatigue syndrome (ME/CFS) is a multisystem disabling disease with unclear etiology and pathophysiology, whose typical symptoms include prolonged debilitating recovery from fatigue or postexertional malaise (PEM). Disrupted production of adenosine triphosphate (ATP), the intracellular energy that fuels cellular activity, is a cause for fatigue. Here, we present a long-term case of ME/CFS: a 75-year-old Caucasian female patient, whose symptoms of ME/CFS were clearly triggered by an acute infection of the Epstein–Barr virus 24 years ago (mononucleosis). Before then, the patient was a healthy professional woman. A recent DNA sequence analysis identified missense variants of mitochondrial respiratory chain enzymes, including ATP6 (ChrMT: 8981A > G; Q152R) and Cox1 (ChrMT: 6268C > T; A122V). Protein subunits ATP6 and Cox1 are encoded by mitochondrial DNA outside of the nucleus: the Cox1 gene encodes subunit 1 of complex IV (CIV: cytochrome c oxidase) and the ATP6 gene encodes subunit A of complex V (CV: ATP synthase). CIV and CV are the last two of five essential enzymes that perform the mitochondrial electron transport respiratory chain reaction to generate ATP. Further analysis of the blood sample using transmission electron microscopy demonstrated abnormal, circulating, extracellular mitochondria. These results indicate that the patient had dysfunctional mitochondria, which may contribute directly to her major symptoms, including PEM and neurological and cognitive changes. Furthermore, the identified variants of ATP6 (ChrMT: 8981A > G; Q152R) and Cox1 (ChrMT: 6268C > T; A122V), functioning at a later stage of mitochondrial ATP production, may play a role in the abnormality of the patient’s mitochondria and the development of her ME/CFS symptoms.

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Virologs, viral mimicry, and virocell metabolism: the expanding scale of cellular functions encoded in the complex genomes of giant viruses

Cited by 11 publications

References 268 publications

Active prokaryotic and eukaryotic viral ecology across spatial scale in a deep-sea brine pool

Active prokaryotic and eukaryotic viral ecology across spatial scale in a deep-sea brine pool

Active prokaryotic and eukaryotic viral ecology across spatial scale in a deep-sea brine pool

Mitochondrial DNA Missense Mutations ChrMT: 8981A > G and ChrMT: 6268C > T Identified in a Caucasian Female with Myalgic Encephalomyelitis/Chronic Fatigue Syndrome (ME/CFS) Triggered by the Epstein–Barr Virus

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