Low Host Abundance and High Temperature Determine Switching from Lytic to Lysogenic Cycles in Planktonic Microbial Communities in a Tropical Sea (Red Sea)

Abstract

The lytic and lysogenic life cycles of marine phages are influenced by environmental conditions such as solar radiation, temperature, and host abundance. Temperature can regulate phage infection, but its role is difficult to discern in oligotrophic waters where there is typically low host abundance and high temperatures. Here, we study the temporal variability of viral dynamics and the occurrence of lysogeny using mitomycin C in a eutrophic coastal lagoon in the oligotrophic Red Sea, which showed strong seasonality in terms of temperature (22.1–33.3 °C) and large phytoplankton blooms. Viral abundances ranged from 2.2 × 106 to 1.5 × 107 viruses mL−1 and were closely related to chlorophyll a (chl a) concentration. Observed high virus-to-bacterium ratio (VBR) (4–79; 16 ± 4 (SE)) suggests that phages exerted a tight control of their hosts as indicated by the significant decrease in bacterial abundance with increasing virus concentration. Heterotrophic bacterial abundance also showed a significant decrease with increasing temperature. However, viral abundance was not related to temperature changes and the interaction of water temperature, suggesting an indirect effect of temperature on decreased host abundance, which was observed at the end of the summertime. From the estimated burst size (BS), we observed lysogeny (undetectable to 29.1%) at low percentages of 5.0% ± 1.2 (SE) in half of the incubations with mitomycin C, while it increased to 23.9% ± 2.8 (SE) when the host abundance decreased. The results suggest that lytic phages predominate, switching to a moderate proportion of temperate phages when the host abundance reduces.

Moderate Seasonal Dynamics Indicate an Important Role for Lysogeny in the Red Sea

“…The BS was assessed from viruses produced during five of the incubations. BS was then calculated by subtracting the produced virus (VPc) in the untreated control samples from the number of produced virus in the virusreduced samples (VPr), which demonstrates the net increase in the number of phages that were released from infected bacteria, and then dividing by the number of bacteria killed (Bdead) during the incubations by infection [26], as follows:…”

“…Reference [25] reported that the high temperature between 31 and 34 • C of the Red Sea was responsible for raising the rates of zooplankton mortality. We tested recently the role of water temperature on viral dynamics and the shift from lysogeny to lytic replication cycles in the Red Sea in a mesotrophic coastal lagoon in the Red Se [26]. The coastal lagoon is a shallow environment separated from the open waters by the reef system, where seawater temperature reached high values (≥33.3 • C) and where we observed that lysogeny occurred in a small percentage at the end of the summer when the temperature was highest and host was low [26].…”

“…Although several studies have been performed on microbial communities and bacteria [27][28][29], studies on viral abundances and dynamics in the Red sea are still limited, addressing communities in coral reefs [30,31] and most recently from shoreline waters of the central Red Sea [32], a coastal lagoon [26] and the coastal waters of the Gulf of Aqaba [33], with all studies indicating complex seasonal patterns of abundance and activity of marine viruses.…”

Modelling the Effects of Traits and Abiotic Factors on Viral Lysis in Phytoplankton

“…The impact of temperature, and understanding whether host maximum growth rate potential affects viral replication, also remain important unknowns; do slow-growing hosts have longer latent periods, or do viruses push the host physiology into overdrive, such that LP is never very long? Winter et al (2012) attempted to use an artificial neural network approach to link intrinsic and extrinsic factors to virus growth dynamics, to rather mixed effect; it did identify the importance of temperature changes, likely linking virus-host dynamics to upshocks in host physiology with temperature increases (Demory et al, 2017;Maat et al, 2017;Ashy and Agusti, 2020;Frenken et al, 2020). Additionally, Mojica and Brussaard (2014, their Table 1) document some temperature interactions with virushost dynamics, but temperature and climate change in general will also affect the type of hosts that dominate both directly and indirectly via impacts on their grazers and nutrient regenerators (Frenken et al, 2020).…”

Picophytoplankton Niche Partitioning in the Warmest Oligotrophic Sea

“…Therefore, the Red Sea offers the opportunity to investigate potential acclimatization and realized adaptation to ocean warming, with a large number of studies addressing its coral reef habitats (Sawall and Al-Sofyani, 2015;Ziegler et al, 2019) and symbionts responses (Hume et al, 2016). It also constitutes a unique opportunity to identify adaptation mechanisms, and physiological and molecular responses to warming (Hume et al, 2016;Giomi et al, 2019;Anton et al, 2020a) including how the elevated temperature may affect biological processes and the interactions between organisms (Hume et al, 2016;Silva et al, 2018;Abdulrahman Ashy and Agustí, 2020;Anton et al, 2020b).…”