Evidence of Trichodesmium viral lysis and potential significance for biogeochemical cycling in the oligotrophic ocean

Abstract

The planktonic cyanobacterium Trichodesmium spp. is a globally important diazotroph, fixing at least 80 Tg N yr -1 in tropical waters. Despite its biogeochemical importance, the mechanisms of Trichodesmium mortality, and the means by which its fixed N enters upper levels of the food web, are poorly understood. Potential virus-like particle (VLP) production by Trichodesmium spp. was observed in both culture (IMS101) and field samples from the tropical North Pacific Ocean, in oceanic waters around the Hawaiian Islands. VLP observed by TEM in IMS101 lysate were approximately 56 nm wide and untailed, and VLP with similar morphology were observed in tissue treated with mit- omycin C. A most-probable number cultivation technique (utilizing bacterized cultures of Tricho- desmium) detected moderate abundances of Trichodesmium-infecting cyanophage (605 to 9750 ml -1 infecting only 1 cultured strain) in 0.2 µm-filtered seawater samples from surface, subsurface and deep chlorophyll maximum samples. Estimation of mortality from virus production was not possible due to rapid VLP release in the first 6 h of dilution incubations. Rather, an indirect approach using burst size (determined from mitomycin C treatment of washed trichomes resuspended in virus-free seawater), decay rate of VLP (from latter part of virus production incubations) and average cyanophage titer was used to estimate mortality. These conservative calculations suggested that 0.3 to 6.5% d -1 (mean = 1.65 ± 0.99% d -1 ) of trichomes could potentially be lysed by viruses, represent- ing the release of approximately 3 to 64% fixed N d -1 . These estimates are based upon a steady-state maintenance of observed VLP abundance, which in nature could be from lysogeny, pseudolysogeny, carrier state, or successive lytic infection. Viral lysis therefore may represent a significant novel mechanism of N release from Trichodesmium spp., even in non-bloom conditions.