Highly enriched N‐containing organic molecules of Synechococcus lysates and their rapid transformation by heterotrophic bacteria

Abstract

Phytoplankton are major contributors of labile dissolved organic matter to marine euphotic zone ecosystems. Viral-mediated phytoplankton lysis releases a considerable amount of bioavailable cellular contents and facilitates localized heterotrophic bacterial growth. The rapid turnover times of this labile organic matter renders it difficult to trace their transformation within natural environments. In the present study, we used a model phototroph-heterotroph coculture system to investigate the organic molecular variation during cyanophageinduced Synechococcus lysis and post-lysis periods using fluorescence spectroscopy and ultrahigh resolution mass spectrometry analyses. Approximately 80% of the Synechococcus lysates were respired to carbon dioxide within 2 days coupled to rapid regeneration of inorganic nutrients. Five fluorescent dissolved organic matter components were detected in the incubations including four humic-like and one protein-like components, and their abundances varied markedly with the succession of the viral lysis process. Viral lysis promoted the transformation of Synechococcus biomass to dissolved organic matter, and heterotrophic bacterial metabolism facilitated the transformation of organic molecules from relatively high (avg.~430 Da) to low (avg.~360 Da) molecular weight, corresponding to variation in their bioavailability. The Synechococcus-derived organic matter was highly enriched in N-containing organic molecules. Identified metabolites within the cultures primarily comprised amino acids or oligopeptides and other low-molecular-weight organic acids, carbohydrates, nucleotides, lipids, biogenic amines, and porphyrins. Among these, oligopeptides, nucleotides, and lipid compounds significantly increased with viral lysis. These results provide insight into biogeochemical cycling mediated by viral shunts in oceans, thus deepening our understanding of microbial food webs at the molecular level. Marine phytoplankton play important roles in global biogeochemical cycles and are major primary producers in euphotic oceans (Falkowski et al. 1998; Field et al. 1998; Azam and Malfatti 2007). Approximately 10% of the carbon fixed by phytoplankton is subsequently released into surrounding seawaters in the form of dissolved organic matter (DOM) via secretion, natural cellular decay, viral lysis, and protistan predation (Azam et al. 1983; Suttle 2007; Fiore et al. 2015). The labile organic matter is then directly taken up and metabolized by heterotrophic bacteria, thereby underlying the marine microbial loop (Azam et al. 1983; Kirchman 2004). Marine picocyanobacteria, including Synechococcus and Prochlorococcus, are the most numerous photosynthetic organisms on Earth and contribute to a quarter of global primary production (Field et al. 1998; Scanlan et al. 2009; Flombaum et al. 2013). Cyanophages that infect cyanobacteria are equally as abundant as their hosts, with up to~20-40% of cyanobacteria being infected and lysed every day in the ocean, thereby coupling the transformation of cyanobacterial

Seasonal Variation in Viral Infection Rates and Cell Sizes of Infected Prokaryotes in a Large and Deep Freshwater Lake (Lake Biwa, Japan)

“…Virus-lysed DOM are regarded as labile for prokaryotic utilization ( Middelboe and Jørgensen, 2006 ) and can be quickly utilized by other heterotrophic prokaryotes ( Zheng et al, 2020 ). Here, we estimated the abundance – using the estimated volume of infected cells – and the contribution of lysed DOM to the DOM pool in Lake Biwa.…”

Opportunistic bacteria with reduced genomes are effective competitors for organic nitrogen compounds in coastal dinoflagellate blooms

“…Previous research on blooms has primarily focused on the microbial community, potential functions, and some chemical signals [7], while only a few studies have been conducted on the composition of DOM, whereas phytoplankton are a major dissolved organic nitrogen (DON) source [32,33]. Cultivated marine Synechococcus is reported to contribute a variety of nitrogen-rich compounds to DOM, including amino acids, oligopeptides as well as nucleosides, and indoles [34,35]. Geider et al [36] found cyanobacteria and diatoms contain 30-60% proteins by dry weight, which are the largest compounds; however, dinoflagellates released more nitrogen-containing substances, while diatoms also released a considerable amount of carbohydrates such as polysaccharides.…”

Changing elemental cycles, stoichiometric mismatches, and consequences for pathogens of primary producers

“…Some viruses infecting phytoplankton have strategies to cope with nutrient limitation within their host, for example, by minimizing interference with N‐fixation (Kuznecova et al 2020) or manipulation of host metabolism to boost N or P uptake (Monier et al 2012, 2017). These strategies can result in a reduced carbon:nutrient content of infected versus healthy host tissue (Ankrah et al 2014), stimulating viral reproduction, but also enriching the quality of the cell material released in the water after cell lysis (Ankrah et al 2014, Zheng et al 2020). Pathogens may indirectly alter plant chemistry by inducing plants to reallocate nutrients as a defense mechanism.…”