Targeted and untargeted lipidomics of Emiliania huxleyi viral infection and life cycle phases highlights molecular biomarkers of infection, susceptibility, and ploidy

Abstract

Marine viruses that infect phytoplankton strongly influence the ecology and evolution of their hosts. Emiliania huxleyi is characterized by a biphasic life cycle composed of a diploid (2N) and haploid (1N) phase; diploid cells are susceptible to infection by specific coccolithoviruses, yet haploid cells are resistant. Glycosphingolipids (GSLs) play a role during infection, but their molecular distribution in haploid cells is unknown. We present mass spectrometric analyses of lipids from cultures of uninfected diploid, infected diploid, and uninfected haploid E. huxleyi. Known viral GSLs were present in the infected diploid cultures as expected, but surprisingly, trace amounts of viral GSLs were also detected in the uninfected haploid cells. Sialic-acid GSLs have been linked to viral susceptibility in diploid cells, but were found to be absent in the haploid cultures, suggesting a mechanism of haploid resistance to infection. Additional untargeted high-resolution mass spectrometry data processed via multivariate analysis unveiled a number of novel biomarkers of infected, non-infected, and haploid cells. These data expand our understanding on the dynamics of lipid metabolism during E. huxleyi host/virus interactions and highlight potential novel biomarkers for infection, susceptibility, and ploidy.

Schrödinger’s Cheshire Cat: Are Haploid Emiliania huxleyi Cells Resistant to Viral Infection or Not?

“…Additionally, a recent study detected novel glycosphingolipids in the haploid E. huxleyi RCC1217 strain, which were similar to the viral GSLs observed in the EhV-infected diploid RCC1216 strain; but the authors did not explain the implications of this observation [21]. Although these GSLs are not yet fully characterized, we suggest that haploid cells are not resistant to infection from viruses.…”

“…The combination of tiling array data, RT-PCR of amplified NCLDV core genes, sequence data, and the viral-like glycosphingolipids present in the haploid cells as discovered by Hunter et al [21] strongly indicates that an active EhV infection is present in the haploid E. huxleyi RCC1217 cells. To establish whether EhV, a DNA virus, is able to exist solely in an RNA form, we searched the EhV genome for the RNA replicase gene.…”

“…We propose that the viral lipids [21] and EhV transcriptome detected in the haploid infer that haploid cells are a unique part of the Coccolithovirus lifecycle, which we propose naming as the Haplococcolithovirocell (HCLVCs) (Figure 6). …”

The remineralization of marine organic matter by diverse biological and abiotic processes

“…While increased TAG production in algae has not been previously linked directly to oxidative stress, increased production has been observed as a response to viral infection in the haptophyte alga Emiliania huxleyi (Hunter et al, 2015).…”

“…Of particular interest to chemical oceanographers and geochemists in this regard are the lipids of marine plankton, biochemicals whose taxonomic specificity and functional diversity make them uniquely suited for use as biomarkers of particular taxa or biogeochemical processes (Close et al, 2013;Pearson, 2014;Rontani et al, 2012;Sturt et al, 2004;Wakeham et al, 1997). Lipids and their many oxidation products are equally useful as indicators of various processes and phenomena in living or senescent biomass (Hunter et al, 2015;Van Mooy et al, 2006;Van Mooy et al, 2009;Vardi et al, 2012). Implicit in the use of these molecules as biomarkers is the recognition that they may be shaped and transformed by diverse catabolic and diagenetic processes in the water column and (when persisting for sufficient time) in sediments (Killops and Killops, 2005).…”