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. 2013 Sep;7(9):1738-51.
doi: 10.1038/ismej.2013.67. Epub 2013 May 2.

Global morphological analysis of marine viruses shows minimal regional variation and dominance of non-tailed viruses

Jennifer R Brum  1 , Ryan O Schenck, Matthew B Sullivan
Affiliations

Global morphological analysis of marine viruses shows minimal regional variation and dominance of non-tailed viruses

Jennifer R Brum et al. ISME J. 2013 Sep.

Abstract

Viruses influence oceanic ecosystems by causing mortality of microorganisms, altering nutrient and organic matter flux via lysis and auxiliary metabolic gene expression and changing the trajectory of microbial evolution through horizontal gene transfer. Limited host range and differing genetic potential of individual virus types mean that investigations into the types of viruses that exist in the ocean and their spatial distribution throughout the world's oceans are critical to understanding the global impacts of marine viruses. Here we evaluate viral morphological characteristics (morphotype, capsid diameter and tail length) using a quantitative transmission electron microscopy (qTEM) method across six of the world's oceans and seas sampled through the Tara Oceans Expedition. Extensive experimental validation of the qTEM method shows that neither sample preservation nor preparation significantly alters natural viral morphological characteristics. The global sampling analysis demonstrated that morphological characteristics did not vary consistently with depth (surface versus deep chlorophyll maximum waters) or oceanic region. Instead, temperature, salinity and oxygen concentration, but not chlorophyll a concentration, were more explanatory in evaluating differences in viral assemblage morphological characteristics. Surprisingly, given that the majority of cultivated bacterial viruses are tailed, non-tailed viruses appear to numerically dominate the upper oceans as they comprised 51-92% of the viral particles observed. Together, these results document global marine viral morphological characteristics, show that their minimal variability is more explained by environmental conditions than geography and suggest that non-tailed viruses might represent the most ecologically important targets for future research.

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Figures

Figure 1
Figure 1
Examples of the four viral morphotypes observed in this study ((a), myovirus; (b), podovirus; (c), siphovirus; (d), non-tailed virus).
Figure 2
Figure 2
(a) Percentage of viral morphotypes in all the surface samples combined, all the DCM samples combined and each oceanic region. Error bars represent s.ds. of the means of all the samples. Letters indicate significant differences between depths or oceanic regions while numbers indicate significant differences within depths or oceanic regions (ANOVA with Tukey's post-hoc test, P<0.001 for all). (b) Box and whisker plots of viral capsid diameters in all the surface samples combined, all the DCM samples combined and each oceanic region. Top, middle and bottom lines of each box correspond to the 75th, 50th (median) and 25th percentiles, respectively. Whiskers extending from the top and bottom of each box correspond to the 90th and 10th percentiles, respectively. Circles represent capsid diameters that are outside of the 90th and 10th percentiles (outliers). Letters indicate significant differences between depths or oceanic regions (ANOVA with Tukey's post-hoc test, P<0.001 for all). The number of viruses used for each data set is given in parentheses.
Figure 3
Figure 3
Ordination of Tara Oceans samples (a) and capsid diameter bins in nm (b) using CA based on distribution of viral capsid diameters with 7 nm bins (s, surface sample; d, DCM sample; surface sample from station 36 is omitted due to missing oxygen data; percentage of total inertia explained by CA1 and CA2 is reported on the axes). Lengths of vectors overlaid on the sample ordination plot correspond to the strength of influence for each environmental variable, with r2 and P-values reported for each vector (c–f). Response surfaces for each environmental variable are also overlaid on the sample ordination plot to assess linearity of the relationship, with r2 (adjusted), P-values and the percentage of deviance explained reported for each response surface (c–f). CA1 was negatively correlated with salinity (Pearson's correlation, r=−0.486, P=0.014) while CA2 was negatively correlated with temperature (Pearson's correlation, r=−0.623, P<0.001) and positively correlated with oxygen (Pearson's correlation, r=0.646, P<0.001).
Figure 4
Figure 4
Box and whisker plots of myovirus, siphovirus and podovirus tail lengths in all the surface samples combined, all the DCM samples combined and each oceanic region. Refer to Figure 2 for a description of box and whisker plot construction. The number of viruses used for each data set is given in parentheses. Letters indicate significant differences between depths (t-test, P=0.001) or oceanic regions (ANOVA on ranks with Dunn's post-hoc test, P<0.05 for all).
Figure 5
Figure 5
Morphological results of all the viruses in this study, including the percentage of each morphotype (a), as well as capsid diameters (b) and tail lengths (c) of all the viruses and each morphotype. The average and s.d. are given for each set of viruses, with ranges reported in parentheses, and the number of viruses analyzed (N) is given for capsid diameters and tail lengths. Refer to Figure 2 for a description of box and whisker plot construction. Letters indicate significant differences between morphotypes (ANOVA on ranks, P<0.001 for all) and numbers indicate significant differences between capsid diameters of non-tailed and all tailed viruses combined (b; Mann–Whitney rank sum test, P<0.001).
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