Impaired viral infection and reduced mortality of diatoms in iron-limited oceanic regions

Abstract

Diatoms contribute up to 40% of marine primary production 1 and have silicified cell walls that ballast substantial vertical flux of particulate organic matter out of the surface into the deep ocean 2 . In high-nutrient, low-chlorophyll regions of the open ocean and along some coastal upwelling margins, iron (Fe) availability limits diatom production [3][4][5] and may contribute to the decoupling of primary productivity and export efficiency in these waters [6][7][8] . Fe-limited waters are biogeochemically distinct, characterized by enhanced drawdown of silicic acid relative to nitrate by Fe-limited diatoms, which leads to high cellular silicon (Si):nitrogen (N) and Si:carbon (C) 9,10 . These regions can also exhibit elevated diatom carbon export efficiency 6-8 and markedly high burial of biogenic silica (bSiO 2 ) relative to organic carbon in underlying sediments 11 . These 'hot spots' of silica burial contribute to widespread limitation of diatom silica production rates in the surface ocean, linking the Fe, Si and C cycles, and may impose a global constraint on the drawdown of atmospheric CO 2 and export production [12][13][14] . Together, these observations underscore the importance of elucidating the underlying chemical, physical and biological interactions that dictate the fate of diatom organic matter and associated elements in the ocean.Viral infection of microbes is a major conduit for elemental cycling in the ocean, transforming the biogeochemical flux of nutrients and carbon, and toggling the balance between export and remineralization processes 15,16 . By fuelling the microbial loop with dissolved organic matter released during host lysis, viruses circumvent the transfer of particulate organic matter to depth or higher trophic levels through the 'viral shunt' 17 . We recently reported accelerated virus-mediated mortality in Si-limited diatoms, demonstrating a role for nutrient availability in facilitating the viral shunt 18 . However viral infection can also 'shuttle' organic matter out of the surface ocean by stimulating processes that facilitate export such as particle aggregation 19,20 and spore formation 21 , highlighting the dynamic, biogeochemical consequences of host-virus interactions. Here we explored diatom host-virus dynamics in Fe-limited regimes of the northeast Pacific Ocean.

Reduced bacterial mortality and enhanced viral productivity during sinking in the ocean

“…For example, an investigation suggested that aggregate formation and vertical carbon fluxes were enhanced by the Coccolithovirus infections of coccolithophore, Emiliania huxleyi , blooms in the North Atlantic [ 86 ]. These indicate that viral infection can “shuttle” surface organic particles into deep waters, and may promote the efficiency of BP in the ocean [ 87 ]. In this study, for the first time, we revealed that environmental changes caused by vertical transplantation decreased the VMM, but significantly increased lytic and lysogenic VP by increasing BS and triggering the switch from the lysogenic to lytic strategy to release additional viral particles into the surrounding water (Fig.…”

Ecological Importance of Viral Lysis as a Loss Factor of Phytoplankton in the Amundsen Sea

“…This so-called viral shuttle was shown in laboratory experiments for diatoms [ 51 ]. For diatoms in iron-limited waters (such as the Southern Ocean), another shuttle system (the so-called viral shuttle) has also recently been suggested, based on a combination of increased silicate in diatom shells and delayed virus-induced mortality [ 116 , 117 ]. Both the viral shunt and viral shuttle, however, would still decrease the trophic transfer efficiency compared to grazing-dominated systems.…”

Diminished carbon and nitrate assimilation drive changes in diatom elemental stoichiometry independent of silicification in an iron-limited assemblage

“…Our finding that none of the dominant diatom genera responded to Fe-limitation by thickening frustules complements previous field studies in both the Equatorial Pacific [ 6 ] and CUZ [ 28 ], lying in stark contrast to studies that suggest diatom frustule thickening is a common response to Fe-limitation [ 2 ]. Thus, evaluation of drivers of carbon export and opal burial in Fe-limited regimes must also consider mechanisms that do not depend on increased silica ballasting, such as increased aggregation [ 77 ], reduced grazing and associated respiratory losses [ 5 ], and viral infection [ 78 ].…”