Re-examining the relationship between virus and microbial cell abundances in the global oceans

Abstract

Marine viruses are critical drivers of ocean biogeochemistry and their abundances vary spatiotemporally in the global oceans, with upper estimates exceeding 108 per ml. Over many years, a consensus has emerged that virus abundances are typically 10-fold higher than prokaryote abundances. The use of a fixed-ratio suggests that the relationship between virus and prokaryote abundances is both predictable and linear. However, the true explanatory power of a linear relationship and its robustness across diverse ocean environments is unclear. Here, we compile 5671 prokaryote and virus abundance estimates from 25 distinct marine surveys to characterize the relationship between virus and prokaryote abundances. We find that the median virus-to-prokaryote ratio (VPR) is 10:1 and 16:1 in the near-and sub-surface oceans, respectively. Nonetheless, we observe substantial variation in the VPR and find either no or limited explanatory power using fixed-ratio models. Instead, virus abundances are better described as nonlinear, power-law functions of prokaryote abundances - particularly when considering relationships within distinct marine surveys. Estimated power-laws have scaling exponents that are typically less than 1, signifying that the VPR decreases with prokaryote density, rather than remaining fixed. The emergence of power-law scaling presents a challenge for mechanistic models seeking to understand the ecological causes and consequences of marine virus-microbe interactions. Such power-law scaling also implies that efforts to average viral effects on microbial mortality and biogeochemical cycles using \"representative\" abundances or abundance-ratios need to be refined if they are to be utilized to make quantitative predictions at regional or global ocean scales.