Diel transcriptional response of a California Current plankton microbiome to light, low iron, and enduring viral infection

Kolody, Bethany; McCrow, John P.; Allen, Lisa Zeigler; Aylward, Frank O.; Fontanez, Kristina M.; Moustafa, Ahmed; Moniruzzaman, Mohammad; Chávez, Francisco P.; Scholin, Christopher A.; Allen, Eric E.; Worden, Alexandra Z.; DeLong, Edward F.; Allen, Andrew E.

doi:10.1038/s41396-019-0472-2

Cited by 64 publications

(96 citation statements)

References 91 publications

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“…Virus proliferation strongly depends on host metabolism (15), often by manipulating the host's metabolic and transcriptional machinery using auxiliary metabolic genes (AMGs) (5,16,17). Additionally, recent environmental studies have reported several viruses infecting marine bacteria to be expressing AMGs in diurnal patterns, coupled with their host metabolism and reproduction cycle (18)(19)(20)(21)(22). Relying on their host for propagation, virus abundance is predicted to follow that of their hosts ("Kill-the-Winner" model (23), and the "Bank" model (24)).…”

Section: Introductionmentioning

confidence: 99%

“…While these concepts have been useful for describing the distribution of viruses in a given sample, our perception of the relationship between temporal abundance variation of marine viruses and host interaction remains largely obscure. Currently only a few environmental studies of diel patterns in marine viruses (18,19,22) and seasonality effects on viral communities (21,(27)(28)(29)(30)(31)(32) have been reported, and none of these incorporate both diel and seasonal time-scales.…”

Section: Introductionmentioning

confidence: 99%

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Rising through the Ranks: Seasonal and Diel Patterns of Marine Viruses

Hevroni

Flores‐Uribe²,

Béjà

et al. 2020

Preprint

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Virus-microbe interactions have been studied in great molecular details for many years in cultured model systems, yielding a plethora of knowledge on how viruses use and manipulate host machinery. Since the advent of molecular techniques and high-throughput sequencing, viruses have been deemed the most abundant organisms on earth and methods such as cooccurrence, nucleotide composition and other statistical frameworks have been widely used to infer virus-microbe interactions, overcoming the limitations of culturing methods. However, their accuracy and relevance is still debatable, as co-occurrence does not necessarily mean interaction. Here, we introduce an ecological perspective of marine viral communities and potential interaction with their hosts, using analyses that make no prior assumptions on specific virus-host pairs. By size fractioning water samples into "free viruses" and "microbes" (i.e. also viruses inside or attached to their hosts) and looking at how viral groups abundance changes over time along both fractions, we show that the viral community is undergoing a change in rank abundance across seasons, suggesting a seasonal succession of viruses in the Red Sea. We use abundance patterns in the different size fractions to classify viral populations, indicating potential diverse interactions with their hosts and potential differences in life history traits between major viral groups. Finally, we show hourly resolved variations of intracellular abundance of similar viral groups, which might indicate differences in their infection cycles or metabolic capacities. marine viruses | seasonal succession | virus-host interaction | diel oscillation

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Rising through the Ranks: Seasonal and Diel Patterns of Marine Viruses

Hevroni

Flores‐Uribe²,

Béjà

et al. 2020

Preprint

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“…S7). We used an additional expression dataset for marine microbial genes (23) to rank KEGG orthologs by their mean expression (18) and found that the 100 most highly expressed KEGG KOs had a significantly higher EEV as compared to the 100 least expressed ones ( Fig. 1D, S8; Mann-Whitney U test P<10 -9 ).…”

Section: Environmental Association Is Stronger In Resource-consuming mentioning

confidence: 99%

“…To estimate codon relative abundance ( ), we counted and sumnormalized codons in all protein-coding genes for each strain. To estimate codon mutation rate ( ( , ′)), we used the published transition:transversion rate of 2:1 for Prochlorococcus and Synechococcus (23).…”

Section: Confounding Effects Between Cost Functions For the Structurementioning

confidence: 99%

Resource conservation manifests in the genetic code

Shenhav

Zeevi

2019

Preprint

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9Ocean microbes are responsible for about 50% of primary production on Earth, and are strongly 10 affected by environmental resource availability. However, selective forces resulting from 11 environmental conditions are not well understood. We studied selection by examining single-12 nucleotide variants in the marine environment, and discovered strong purifying selective forces 13 exerted across marine microbial genes. We present evidence indicating that this selection is 14 driven by the environment, and especially by nitrogen availability. We further corroborate that 15 nutrient availability drives this 'resource-driven' selection by showing stronger selection on highly 16 expressed and extracellular genes, that are more resource-consuming. Finally, we show that the 17 standard genetic code, along with amino acid abundances, facilitates nutrient conservation by 18 providing robustness to mutations that increase nitrogen and carbon consumption. Notably, this 19 robustness generalizes to multiple taxa across all domains of life, including the Human genome, 20 and manifests in the code structure itself. Overall, we uncover overwhelmingly strong purifying 21 selective pressure across marine microbial life that may have contributed to the structure of our 22 genetic code. 23 could be attributed to the different rates of synonymous mutations between the high-and low-595 nitrate groups, which, combined with simplex properties, may affect observed nonsynonymous

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“…Deep sequencing approaches have become widely used in marine meta-omics and are effective for studying abundant community members, genes, and transcripts [50][51][52][53][54]. Alternatively, high-resolution microarrays have advantages for detecting rare community members and for differentiating among closely related strains [55][56][57].…”

Section: Introductionmentioning

confidence: 99%

Phytoplankton transcriptomic and physiological responses to fixed nitrogen in the California current system

et al. 2020

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Marine phytoplankton are responsible for approximately half of photosynthesis on Earth. However, their ability to drive ocean productivity depends on critical nutrients, especially bioavailable nitrogen (N) which is scarce over vast areas of the ocean. Phytoplankton differ in their preferences for N substrates as well as uptake efficiencies and minimal N requirements relative to other critical nutrients, including iron (Fe) and phosphorus. In this study, we used the MicroTOOLs high-resolution environmental microarray to examine transcriptomic responses of phytoplankton communities in the California Current System (CCS) transition zone to added urea, ammonium, nitrate, and also Fe in the late summer when N depletion is common. Transcript level changes of photosynthetic, carbon fixation, and nutrient stress genes indicated relief of N limitation in many strains of Prochlorococcus, Synechococcus, and eukaryotic phytoplankton. The transcriptomic responses helped explain shifts in physiological and growth responses observed later. All three phytoplankton groups had increased transcript levels of photosynthesis and/or carbon fixation genes in response to all N substrates. However, only Prochlorococcus had decreased transcript levels of N stress genes and grew substantially, specifically after urea and ammonium additions, suggesting that Prochlorococcus outcompeted other community members in these treatments. Diatom transcript levels of carbon fixation genes increased in response to Fe but not to Fe with N which might have favored phytoplankton that were co-limited by N and Fe. Moreover, transcription patterns of closely related strains indicated variability in N utilization, including nitrate utilization by some highlight adapted Prochlorococcus. Finally, up-regulation of urea transporter genes by both Prochlorococcus and Synechococcus in response to filtered deep water suggested a regulatory mechanism other than classic control via the global N regulator NtcA. This study indicated that co-existing phytoplankton strains experience distinct nutrient stresses in the transition zone of the CCS, an understudied region where oligotrophic and coastal communities naturally mix.

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Diel transcriptional response of a California Current plankton microbiome to light, low iron, and enduring viral infection

Cited by 64 publications

References 91 publications

Rising through the Ranks: Seasonal and Diel Patterns of Marine Viruses

Rising through the Ranks: Seasonal and Diel Patterns of Marine Viruses

Resource conservation manifests in the genetic code

Phytoplankton transcriptomic and physiological responses to fixed nitrogen in the California current system

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