Food, Mortality or Temperature? What Matters Most for Heterotrophic Bacteria in the Tropical Upper Ocean

Disentangling the effects of temperature, bottom-up (resource availability) and top-down (viral lysis and protistan grazing) controls on the biomass and growth rates of heterotrophic bacterioplankton has remained challenging, especially in the underexplored tropical and subtropical oceans. Here we combine a dataset gathered in the subtropical and tropical Atlantic, Indian and Pacific oceans with inshore and offshore surface observations in the central Red Sea, a substantially warmer (28.8 ± 0.4°C) basin compared with the other sites (24.7 ± 0.2°C). Heterotrophic bacteria and phytoplankton stocks covaried positively except in the Red Sea, which showed significantly lower bacterial abundances (typically <5 x 106 cells mL-1). Oligotrophy was shared among all sites, characterized by similar chlorophyll a and inorganic and organic nutrient concentrations. The higher relative abundances of viruses and heterotrophic nanoflagellates in the Red Sea suggest a tight top-down control preventing the accumulation of larger bacterial numbers. Red Sea bacteria showed variable specific growth rates but almost 2-fold higher than their oceanic counterparts (0.81 vs. 0.47 ± 0.03 d-1) and were less responsive to temperature than to trophic state. The contribution of the typically copiotrophic high nucleic acid content cells explained 41% of the variance in specific growth rates of the pooled dataset. We suggest that the balance between widespread resource limitation and local peaks in protistan and viral mortality will largely impact potential future temperature-driven increases in heterotrophic bacteria biomass in low latitude waters.