Top‐down controls on nutrient cycling and population dynamics in a model estuarine photoautotroph–heterotroph co‐culture system

Abstract

Viral lysis and protistan grazing are thought to be the major processes leading to microbial mortality in aquatic environments and thus regulate community diversity and biogeochemical cycling characteristics. Here, we studied nutrient cycling and bacterial responses to cyanophage-mediated photoautotroph lysis and ciliate predation in a model Synechococcus-heterotroph co-culture system. Both viral lysis and Euplotes grazing facilitated the transformation of organic carbon from biomass to dissolved organic matter with convention efficiencies of 20%-26%. The accumulation of ammonium after the addition of phages and ciliates suggested the importance of recycled NH 4 + occurred in the interactions between Synechococcus growth and heterotrophic bacterial metabolism of photosynthate. The slower efficiency of P mineralization compared to N (primarily ammonium) indicated that P-containing organic matter was primarily integrated into bacterial biomass rather than being remineralized into inorganic phosphate under C-rich conditions. In the cyanophage addition treatment, both Fluviicola and Alteromonas exhibited rapid positive responses to Synechococcus lysing, while Marivita exhibited an apparent negative response. Further, the addition of Euplotes altered the incubation system from a Synechococcus-driven phycosphere to a ciliate-remodelled zoosphere that primarily constituted grazing-resistant bacteria and Euplotes symbionts. Top-down controls increased co-culture system diversity and resulted in a preference for free-living lifestyles of dominant populations, which was accompanied by the transfer of matter and energy. Our results indicate topdown control was particularly important for organic matter redistribution and inorganic nutrient regeneration between photoautotrophs and heterotrophs, and altered bacterial lifestyles. This study consequently sheds light on marine biogeochemical cycling and the interaction networks within these dynamic ecosystems.

Phage strategies facilitate bacterial coexistence under environmental variability

“…Their abundance and distribution are linked to their hosts ( Clokie et al, 2011 ). Phages can promote bacterial diversity by acting as a top-down control for highly abundant species ( Thingstad, 2000 ; Ram, Keshri & Sime-Ngando, 2020 ; Zheng et al, 2021 ). Furthermore, phages can influence their host by gene transfer ( Day et al, 2017 ) or reprogramming of the host’s gene expression and metabolism ( Long, Patterson & Paul, 2007 ; Hurwitz & U’Ren, 2016 ).…”

Comparison and interpretation of freshwater bacterial structure and interactions with organic to nutrient imbalances in restored wetlands

“…Our findings were consistent with those of several previous studies ( Aanderud et al, 2018 ; Jabir et al, 2020 ). Bacterial taxa form several microbiotas (modules) based on their connections and interactions, which may be due to similar nutritional preferences or resource complementarity ( Zheng et al, 2021 ). Furthermore, more nodes and connections appeared in the low-COD/N and high-N/P groups ( Figures 7A,B ).…”

Viral infection of an estuarine Synechococcus influences its co-occurring heterotrophic bacterial community in the culture

“…The cyanophage samples were stained with SYBR Green I (Invitrogen) at a final concentration of 0.005% v/v for 10 min at 80°C in the dark and cooled at room temperature for 5 min. The microbial abundance data was acquired and analyzed by the EXPOTM 32 MultiCOMP flow cytometry analysis software and FCM Express software (Cai et al, 2015;Zheng et al, 2021b). The abundance of Synechococcus was calculated according to the method described by Jiao et al (2002), and cells were detected from plots of side scatter versus red fluorescence signals and orange fluorescence versus red fluorescence signals (Jiao et al, 2005;Zheng et al, 2018Zheng et al, , 2021bWang et al, 2019).…”

“…Marine picocyanobacterial isolate cultures (including Synechococcus and Prochlorococcus) usually contain heterotrophic bacteria (Moore et al, 2007;Cole et al, 2014;Zheng et al, 2018Zheng et al, , 2021bCruz and Neuer, 2019), which may be grabbed from the natural habitat during the picocyanobacterial isolation (Zheng et al, 2021a). Many picocyanobacteria grow more efficiently when cocultured with heterotrophic bacteria instead of being in axenic cultures (Hayashi et al, 2011;Shen et al, 2011;Cole et al, 2014).…”

“…It is reported that, among the co-occurring heterotrophic bacteria in a Synechococcus culture, specific species of Alphaproteobacteria and Flavobacteria are responsible for the organic compound transformation from high molecular weight (HMW) to low molecular weight (LMW) (Zheng et al, 2020), which is also congruent with the rapid rise of Alphaproteobacteria and Flavobacteria in a coastal bacterial community in response to the introduction of Synechococcus-derived DOM which is rich in HMW molecules (Xie et al, 2020;Wang et al, 2022). Therefore, picocyanobacteriaheterotroph cocultures can be used as model microcosms to simulate and investigate microbial interactions in the natural marine environment (Zheng et al, 2021b).…”