Viral Lysis Alters the Optical Properties and Biological Availability of Dissolved Organic Matter Derived from Prochlorococcus Picocyanobacteria

Abstract

Phytoplankton contribute almost half of the world's total primary production. The exudates and viral lysates of phytoplankton are two important forms of dissolved organic matter (DOM) in aquatic environments and fuel heterotrophic prokaryotic metabolism. However, the effect of viral infection on the composition and biological availability of phytoplankton-released DOM is poorly understood. Here, we investigated the optical characteristics and microbial utilization of the exudates and viral lysates of the ecologically important unicellular picophytoplankton Prochlorococcus. Our results showed that Prochlorococcus DOM produced by viral lysis (Pro-vDOM) with phages of three different morphotypes (myovirus P-HM2, siphovirus P-HS2 and podovirus P-SSP7) had higher humic-like fluorescence intensities, lower absorption coefficients and higher spectral slopes compared to DOM exuded by Prochlorococcus (Pro-exudate). The results indicate that viral infection altered the composition of Prochlorococcus-derived DOM and might contribute to the pool of oceanic humic-like DOM. Incubation with Pro-vDOM resulted in a greater dissolved organic carbon (DOC) degradation rate and decreases in the absorption spectral slope and heterotrophic bacterial growth rate compared to incubation with Pro-exudate, suggesting that Pro-vDOM was more bioavailable compared to Pro-exudate. In addition, the stimulated microbial community succession trajectories were significantly different between the Pro-exudate and Pro-vDOM treatments, indicating that viral lysates play an important role in shaping the heterotrophic bacterial community. Our study demonstrated that viral lysis altered the chemical composition and biological availability of DOM derived from Prochlorococcus, which is the numerically dominant phytoplankton in the oligotrophic ocean. Importance The unicellular picocyanobacterium Prochlorococcus is the numerically dominate phytoplankton in the oligotrophic ocean, contributing to the vast majority of marine primary production. Prochlorococcus releases a significant fraction of fixed organic matter into surrounding environment and supports a vital portion of heterotrophic bacterial activity. Viral lysis is an important biomass loss process of Prochlorococcus. Yet little is known about whether and how viral lysis affects Prochlorococcus-released dissolved organic matter (DOM). Our paper shows that viral infection alters the optical properties (such as the absorption coefficients, spectral slopes and fluorescence intensities) of released DOM and might contribute to a humic-like DOM pool and carbon sequestration in the ocean. Meanwhile, viral lysis also releases various intracellular labile DOM including amino acids, protein-like DOM and lower-molecular weight DOM, increases the bioavailability of DOM and shapes the successive trajectory of the heterotrophic bacterial community. Our study highlights the importance of viruses in impacting the DOM quality in the ocean.

Distribution, spectral characteristics, and seasonal variation of dissolved organic matter in the northern Beibu Gulf, South China Sea

“…The paired data including DOC, CDOM, and FDOM and unpaired data (only DOC) are denoted by circles and squares, respectively. Tanoue, 2003;Xiao et al, 2021). Coupled with the negative relationships between C3 intensity and AOU in this region in spring and summer (r = −0.65, p <.001), we conclude that protein-like C3 is degraded by bacteria in estuaries.…”

“…Specifically, FDOM excitation-emission matrices (EEMs) coupled with parallel factor (PARAFAC) analysis are used to characterize the natural DOM in numerous estuaries and coastal gulfs around the world, such as the Yangtze River estuary (Guo et al, 2014), Pearl River estuary (Li et al, 2019), Jiulong River estuary (Guo et al, 2011), Taiwan estuaries (Yang et al, 2013b), Gulf of Mexico (Yamashita et al, 2015), and Gulf of Alaska (Dainard and Gueǵuen, 2013). The humic-like components tend to be resistant to microbial use but are sensitive to solar radiation (Rochelle-Newall and Fisher, 2002;Helms et al, 2013), whereas the protein-like components are rapidly consumed by microorganisms (Xiao et al, 2021). Thus, bulk DOC combined with its specific optical properties can provide valuable information regarding the quantity, quality, and biogeochemical reactivity of DOM in natural aquatic environments.…”

Disentangling top-down drivers of mortality underlying diel population dynamics ofProchlorococcusin the North Pacific Subtropical Gyre

“…However, particle aggregation could be stimulated via processes such as sloppy feeding or viral lysate [28, 45]. As viral lysate from picocyanobacteria is partially labile [46, 47] aggregation and sinking could be stimulated indirectly by viral lysate via heterotrophic bacterial growth. Particle attachment and aggregation could also be stimulated by TEP (Transparent exopolymer particles), which is produced in xenic Prochlorococcus cultures [48, 49].…”

Abundant and cosmopolitan lineage of cyanopodoviruses lacking a DNA polymerase gene

“…In the ocean 1%-15% of marine cyanobacteria are infected by cyanophages [17,18], and in some oceanic regions more than 46% of cyanobacteria can be killed by phages daily [19]. Via infection, cyanophages could greatly impact the population size, community dynamics [18,20,21], genome diversity and evolution of cyanobacteria [22,23], as well as marine biogeochemical cycles [24][25][26][27][28]. Marine cyanophages isolated thus far include several distinct groups: cyanopodoviruses belonging to the T7-like group, cyanomyoviruses belonging to the T4-like or TIM5-like groups, and cyanosiphoviruses [29][30][31][32][33][34][35].…”