Virus-host coexistence in phytoplankton through the genomic lens

11 pages, 5 figures, 1 table, supplementary materials http://advances.sciencemag.org/cgi/content/full/6/14/eaay2587/DC1.-- Data and materials availability: The genome sequence for O. mediterraneus RCC2590 and OmV2 can be found under GenBank accession numbers WMKK00000000 and MN688676, respectively. The complete gene annotations of RCC2590 can be accessed on ORCAE (https://bioinformatics.psb.ugent.be/orcae/). MMETSP sequence data can be accessed from www.imicrobe.us/#/projects/104. The genomes and their GenBank accession numbers used in this study are as follows: B. prasinos (GCA_002220235.1), M. commoda RCC299 (GCA_000090985.2), M. pusilla CCMP1545 (GCA_000151265.1), O. tauri RCC4221 (CAID01000001.2 to CAID01000020.2, CR954200.2, and CR954199.2), O. lucimarinus CCE9901 (GCA_000092065.1), BpV1 (HM004432.1), BpV2 (HM004430.1), MpV1 (HM004429.1), OtV1 (FN386611.1), OtV2 (FN600414.1), OtV5 (EU304328.2), OtV6 (JN225873.1), OlV1 (HM004431.1), OlV2 (KP874736.1), OlV3 (HQ633060.1), OlV4 (JF974316.1), OlV5 (HQ632827.1), OlV6 (HQ633059.1), OlV7 (KP874737.1), and OmV1 (KP874735.1). Ostreococcus sp. RCC809 is available from the JGI Genome Portal under project ID 16233
Virus-microbe interactions in the ocean are commonly described by “boom and bust”dynamics, whereby a numerically dominant microorganism is lysed and replaced by a virus-resistant one. Here, we isolated a microalga strain and its infective dsDNA virus whose dynamics are characterized instead by parallel growth of both the microalga and the virus. Experimental evolution of clonal lines revealed that this viral production originates from the lysis of a minority of virus-susceptible cells, which are regenerated from resistant cells. Whole-genome sequencing demonstrated that this resistant-susceptible switch involved a large deletion on one chromosome. Mathematical modeling explained how the switch maintains stable microalga-virus population dynamics consistent with their observed growth pattern. Comparative genomics confirmed an ancient origin of this “accordion” chromosome despite a lack of sequence conservation. Together, our results show how dynamic genomic rearrangements may account for a previously overlooked coexistence mechanism in microalgae-virus interactions.
This research was funded by the ANR grants REVIREC ANR-12-BSV7-0006-01, DECOVIR ANR-12-BSV7-0009, and PHYTNESS ANR-13-JSV6-0005. E.V. is funded by BOF project GOA 01G01715, and L.F.B. is funded by the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement no. H2020-MSCA-ITN-2015-675752
With the funding support of the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S), of the Spanish Research Agency (AEI)