Abstract
Although we have gained insight into the biological and biochemical effects of natural sunlight exposure on prokaryotes, little is known about sunlight exposure on natural virus communities. To address this question, an investigation of the effects of sunlight and dark treatments on viral communities, viral production and decay rates in Kenting coastal waters was conducted. The average rate of net viral production in the sunlight and dark treatment was 0.010 and 0.018 × 106 viruses mL–1 h− 1, respectively. Furthermore, averaged value for viral decay in the sunlight treatment was 0.016 × 106 viruses mL− 1 h− 1, a significant decrease (ca. 60%=((0.83 − 0.33)/(0.83 × 100%)) was observed in sunlight conditions, whereas no significant changes occurred in dark conditions. The gross viral production under sunlight conditions was slightly higher, however, non-significantly higher than that in the dark treatment. As a result, we suggest that sunlight damages a large portion of the natural viral community, affecting the role viruses play in food webs.
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1 Introduction
Over the past three decades, viruses have been extensively studied in marine surface waters for their ecological roles (Fuhrman 1999; Weinbauer 2004). Viruses in the oceans contribute significantly to the mortality of a wide range of organisms and impact the biogeochemical cycles of the oceans (Wommack and Cowell 2000; Suttle 2005). Studies in the field have shown that viral counts correlate much better with bacterial abundance than with chlorophyll a. While viruses that infect eukaryotes certainly exist, they are thought to most commonly infect bacteria (Wommack and Cowell 2000).
There have been a number of studies examining the effect of sunlight radiation on natural bacterial communities (Kaiser and Herndl 1997; Sommaruga et al. 1997; Jeffrey et al. 2000; Alonso-Sáez et al. 2006; Ruiz-González et al. 2012; Teira et al. 2019). The effects of natural solar UV exposure on marine bacteria include reduced abundances of bacteria (Pakulski et al. 1998; Bertoni et al. 2011), amino acid uptake (Bailey et al. 1983), and a significant reduction of protein and DNA synthesis (Sommaruga et al. 1997). Due to their small size, bacteria do not have the ability to develop effective photoprotection against UV radiation (Garcia-Pichel 1994). Therefore, bacteria are probably the most vulnerable group to photodamage in the plankton. Although we have gained insight into the biological and biochemical effects of UV exposure on prokaryotes, little is known about UV exposure on natural virus communities.
Viral production is counterbalanced by viral losses due to nanoflagellate grazing and viral decay (Fuhrman and Noble 1995). Viral decay in sunlit surface waters is primarily determined by UV radiation, particle adsorption, and temperature (Mojica and Brussaard 2014). In the last decade, extensive research has shown that UV radiation damages DNA-containing viruses in marine environments. The findings of earlier studies based on isolates (Wommack et al. 1996; Wilhelrn et at. 1998) as well as natural virus communities (Wilhelrn et at. 1998; Bettarel et al. 2002; Wilhelm et al. 2002a, b) have suggested that solar radiation can contribute to the destruction of infectivity in natural virus communities at the ocean surface. According to study of Suttle and Chen (1992), virus decay rates are significantly higher in areas with high amounts of sunlight, and other studies found UV damage to be one of the most significant factors that contribute to viral decay (Noble and Fuhrman 1997). While some viruses decay rapidly when subjected to full sunlight at a rate of 40–80% per hour (Suttle and Chen 1992), other viruses decay at a slow rate of only 5–10% per hour (Wommack et al. 1996); thus, generalizations cannot be made.
An accurate analysis of viral dynamics must include independent measurements of both viral production (VP) and decay (VD). In this study, independent measurements were carried out in the dark and in full sunlight to test the effect of sunlight and dark on viral dynamics and whether the steady-state assumption is reflected in situ in diel conditions. We found that there was a significant difference in viral production and decay between dark and sunlight treatments.
2 Materials and methods
2.1 Sampling
In the southern Taiwan coast area (22°02.07’N, 120°41.3E) surface waters were sampled on 21 May 2022 from an established station in Kenting. We gently poured surface water into 10 L polypropylene carboys after collecting it with a bucket. Water temperature was measured during casting, and samples were deposited in the lab within 30 min.
2.2 Viral production and viral decay rate experiments
Water samples were transferred immediately after collection into polypropylene carboys and then subjected to the following treatments. In this study, we used two different methods in order to estimate the viral production rate and its decay rate. A dilution technique, developed by Wilhelm et al. (2002ab), was used to estimate VP. Firstly, we first prepared the grazing-free water by vacuum-filtering 1 L of surface seawater through a 47 mm diameter and 2 μm pore-size polycarbonate track-etched filter membrane (Whatman) before performing the experiments. The size fractionation used for grazing-free water (< 2 μm) was chosen to eliminate nanoflagellates but not bacteria. Secondly, in order to generate virus-free water for viral dilution, 200 mL of grazer-free seawater was passed through a Minimate TFF Capsule (Pall) with a molecular weight cut-off of 30 kDa. Finally, the virus-free water was mixed with 50 mL of grazer-free water to dilute the abundance of bacteria and viruses. This resulted in bacteria and viruses being diluted to approximately 20% of their initial abundance. This made it possible to count the number of phages released from the bacteria, greatly reducing the possibility of bacterial infection. A 50 mL plastic tube was filled with the diluted incubation water and thoroughly mixed.
The viral decay rate (VD) was determined by using the approach of Noble and Furhman (1997). Briefly, water samples were filtered through polycarbonate filters with a pore size of 0.2 μm to remove bacteria and particles > 0.2-µm. The filtration-based method for estimating VD is based on the removal of bacteria, thus we assume the function of infectivity could not appear in this system. Furthermore, triplicates (50 mL) were made and incubated with VP experiments. VD measurements began following the appearance of a significant decrease in viral abundance. From the decrease in viral abundance over time, the viral decay was calculated by fitting a linear regression to the viral abundance versus time.
As a dark treatment, the tubes were covered with aluminum foil, and all tubes were then moved outside of the laboratory immediately after preparation and were incubated for 24 h under natural light, in a thermo-controlled incubator that controlled the in situ temperature. All the treatments were performed in triplicates. In order to detect bacterial and viral abundances, 1 mL subsamples were collected at the beginning of the experiment as well as every 2 h for the following 24 h.
Linear regression between viral density and incubation time was used to calculate net viral production (NVP) and VD. Viral abundance exhibits a significant linear relationship with incubation time, and NVP and VD are determined by the slope of the regression (viruses mL− 1 h− 1) (Mei and Danovaro 2004). As a result of measuring net viral production and viral decay, we can estimate gross viral production (the sum of net viral production and viral decay), which can represent the total number of viruses produced h− 1 by infected bacteria. Based on the patterns of NVP and VD observed during the study period, we estimated gross viral production (GVP) as the sum of NVP and VD. (the equation is “Net viral production (NVP) = Gross viral production (GVP)-Decay rate (VD)”).
2.3 Bacterial growth rate
The VP culture contained approximately 20% of natural abundance of bacteria and viruses due to dilution procedures. The assumption that the viral infection was neglected because low contact rates between viruses and bacteria in the VP experiments. Furthermore, in order to get a better understanding of how the sunlight and dark condition affect bacterial growth in the VP experiments, the bacterial growth rate was measured in the 20% diluted (viruses-free water diluted with < 2 μm filtered waters) samples. The bacterial growth rate was calculated as follows:
µ = ln (Nt/N0)/t.
where µ is the growth rate (h− 1), N0 and Nt are the abundance of bacteria at the beginning and end of incubation, and t is the incubation time.
2.4 Enumeration of virus and bacterial abundance by flow cytometry (FCM)
Viral subsamples of 0.5 mL were collected every 2 h from each incubation set up and fixed in glutaraldehyde (0.5% final concentration) at 4 °C for at least 15 min and subsequently deep-frozen in liquid nitrogen. Bacterial subsamples (1 mL) were also collected every 2 h from each incubation and fixed in paraformaldehyde (1% final concentration). Virus and bacterial samples were preserved at -80 °C until FCM analysis.
Viral and bacterial samples were analyzed using a CytoFLEX S flow cytometer (Beckman Coulter, Indianapolis) equipped with a 488 nm air-cooled argon-ion laser, a standard 525 nm filter, and an SYBR signal trigger. Prior to staining, viral samples were diluted 1:10 in Tris-EDTA (TE) buffer (pH 8.0, EM grade) to minimize the interference from high particle density. The diluted samples were stained with SYBR Green I (final concentration 1:50,000 of commercial stock) and incubated in the dark at 80 °C for 10 min. After staining, samples were cooled to 25 °C in an ice bath and processed through FCM as per the method by Brussaard (2004). Blank controls of TE buffer stained with the same concentration of SYBR Green I were run for detecting and eliminating any noise from the buffer. Bacterial samples were stained with SYBR Green I (final concentration 1:10,000) for 15 min in the dark and processed through FCM according to the protocol of Hammes and Egli (2010).
2.5 Statistical analysis
The relationship between viral abundance and time for triplicate incubations was analyzed using linear regression analysis. Significance of the regression lines was tested using analysis of variance (ANOVA). STATISTICA 7.0 software was used for all statistical operations. A probability value of < 0.05 was considered significant.
3 Results
It is estimated that bacterial and viral abundance was 2.4 × 105 cells mL–1 and 1.3 × 106 viruses mL–1 during the study period, respectively. In this study, we also reported new data on various viral parameters (viral production and viral decay rate). A linear increase in viral abundance was observed in the sunlight and dark treatment as expected in the diluted experiment (Fig. 1A, B). The average rate of net viral production in the sunlight and dark treatment was 0.010 and 0.018 × 106 viruses mL–1 h− 1, respectively.
As for VD experiments, averaged value for viral decay in the sunlight treatment was 0.016 × 106 viruses mL− 1 h− 1 (Fig. 2A). However, the regression slope for dark decay incubations was not significant (p > 0.05) and viral decay was not determined in this dark treatment (Fig. 2B). Under natural sunlight treatment, gross viral production was 0.026 × 106 virus mL− 1 h− 1 (Table 1). Furthermore, we estimated that the gross viral production was 0.018 × 106 virus mL− 1 h− 1 in the dark treatment (Table 1). The gross viral production under sunlight conditions was slightly higher, however, non-significantly higher than that in the dark treatment (t-test, p > 0.05).
During the study period, bacterial abundance increased from 0.51 × 105 to 22.1 × 105 cells mL− 1 and 0.59 × 105 to 29.7 × 105 cells mL− 1 in sunlight and dark treatment, respectively. We found bacterial abundance was slightly higher after 24 h in dark incubation (Fig. 3). However, analysis of this studies of bacterial growth in natural sunlight and dark treatments, found that bacterial growth rates were not significantly different among the treatments (t-test, p > 0.05), with a mean growth rate of 0.18 and 0.20 h− 1 in sunlight and dark conditions, respectively (Fig. 3A, B).
4 Discussion
New data on viral parameters (viral production and viral decay rate) were obtained in this study under natural sunlight and in complete dark. A better understanding of the viral dynamics in aquatic environments requires detailed analyses of viral production and decay and the viral balance. Our results indicate that a significant difference between sunlight and dark treatments in viral production and decay rates. It was observed that viral abundance increased significantly in the dilution approach under dark condition, while it increased only slightly in the sunlight conditions (Fig. 1). As a result of viral decay experiments, a significant decrease (ca. 60%=((0.83 − 0.33)/(0.83 × 100%)) was observed in sunlight conditions, whereas no significant changes occurred in dark conditions (Fig. 1).
A dilution method was used to estimate viral production using prefiltered (virus-free) seawater, diluted with seawater samples. We can compare our results to most of the available information because this method is relatively simple and widely used in literature (Mei and Danovaro 2004; Wilhelm et al. 2002a, b). In our preliminary study, we tested VP culture containing approximately 20% and 50% of natural abundance of bacteria and viruses during the 24 h incubation experiments (Fig. 4). In the 20% and 50% diluted treatments, the average viral production rate was 0.029 and 0.012 × 106 viruses mL–1 h− 1, respectively (Fig. 4). At the end of the experiment, viral abundance was higher in 20% diluted samples than in 50% diluted samples (Fig. 4). According to the research, the 20% diluted samples exhibit a significantly higher VP compared to 50% diluted samples due to the reduced possibility of bacterial infection during the study period. To date, most studies have concentrated on the heterotrophic bacterial community, and have thus incubated in dark condition (Mei and Danovaro 2004; Wilhelm et al. 2002a, b). The other question usually raised concern is whether the incubations should be carried out under in situ light levels or under dark. Virus production may be favored in photoheterotrophs incubated in situ under light conditions, although light effects may cause virus loss. Sunlight is well known for its direct and significant effect on the inactivation of viruses, and these studies provide quantitative information on sunlight-induced DNA damage in natural virus communities (Suttle and chen 1992; Noble and Fuhrman 1997; Weinbauer et al. 1999).
It is essential to determine the rate at which viruses are produced and decayed independently in order to perform a thorough analysis of viral dynamics. By balancing viral production and decay, biomass and community composition of viruses are determined and virus-host interactions are affected, directly impacting microbial communities and biogeochemical cycles (Jiao et al. 2010). According to Fig. 1 in this study, the estimated net virus production rates differ significantly between sunlight and dark incubations. A major difference between them is that natural virus communities are more susceptible to sunlight-induced viral decay (Fig. 2). Our results throughout this study indicate that viral losses through viral decay counterbalances gross viral production under sunlight incubation (Fig. 2). UV radiation has been shown to cause damage to DNA-containing viruses in marine environments over the last decade (Jeffrey et al. 2000). A similar experiment was performed in which seawater samples were incubated in sunlight, in the dark, or under glass to allow the causative agents of virus decay to be partitioned (Noble and Fuhrman 1997), and suggested that sunlight is an important contributing factor to virus decay. Several other factors contributed to the decay rate reduction, including filtration, and heat-labile, high-molecular-weight dissolved material (> 30 kDa, probably enzymes) appeared responsible for about 1/5 of the maximum decay rate (Noble and Fuhrman 1997). Based on the findings above, sunlight contributes substantially to virus decay. However, particles and dissolved substances in seawater play an important role as well. In the present study, we estimated viral decay by filtration-based method (Noble and Fuhrman 1997) that is based on the removal of bacteria, aggregates, and suspended particles and may result in a lower rate of virus removal through this incubation system. Hence, viral decay rates in this study may have been partially underestimated with this method. It has been shown that viruses are important in the biogeochemical cycling of carbon and nitrogen in the ocean (Fuhrman 1999; Suttle 2007), but the viral loss was caused by sunlight exposure at the surface, which partially decreased viral effects on bacteria and indirectly reduced bacterial mortality.
As a result of measuring net viral production (NVP) and viral decay (VD), we may be able to estimate gross viral production (GVP) (the sum of net viral production and viral decay), which could represent the total number of viruses produced by infected bacteria per hour. Previous experiments indicate that a higher viral production rate through higher rates of bacterial production and host cell metabolic activities (Bongiorni et al. 2005). Similarly, some studies have found that viral production correlates significantly with prokaryotic heterotrophic production (Hewson and Fuhrman 2003; Danovaro et al. 2008), and further confirmed the metabolic activity of the prokaryotes appears to be the primary determinant of viral production. However, in this study, we found bacteria grew at similar rates under sunlight and dark incubation (Fig. 3). However, another interesting observation from the continuous culture experiments was there was higher GVP and detectable lower bacterial abundance after 24 h sunlight culture experiment. According to our results, decreasing bacterial abundance leads to higher virus release under sunlight condition. Moreover, similar to our study, Weinbauer et al. (2010) did not find significant differences in estimated virus production rates between light and dark incubations. It is certainly possible that some virus populations increased in production while others were lost in the contrast between light and dark incubation, despite the fact that changes in virus community structure were not examined in this study.
5 Conclusion
We confirm earlier findings based on isolates (Suttle and Chen 1992; Wommack et al. 1996; Suttle and Chan 1994) and natural virus communities (Wilhelrn et al. 1998; Weinbauer et al. 1999; Garza and Suttle 1998) that sunlight causes the loss of viral communities and the destruction of their infectivity. Several conclusions can be drawn from the data presented in this paper. First, as a result, sunlight damages a large portion of the natural viral community, affecting the role viruses play in food webs. Based on these data, viral decay may influence nutrient regeneration and is therefore an important factor to consider when considering carbon and nutrient cycling. Second, using direct sunlight incubation in this study showed slightly higher gross viral production than that under dark, possibly because metabolic activities of bacteria are higher under direct sunlight. A caveat to this is that we did not examine changes in the virus community structure. For example, some virus populations may have increased, while others may have decreased when incubated in light or dark.
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The research was conducted in the frame of the Russian state assignments No. 121040600178-6, AAAA-A21-121121700354-9 and supported by RFBR projects 18-44-920026 (works on the GAF phenomenon) and 21-55-52001, and the Ministry of Science and Technology, ROC (Taiwan), grant number NSC 109-2611-M-019-013 and MOST 111-2119-M-019-002.
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Conceptualization: A-YT; methodology: A-YT; PW-YC; MO; validation: A-YT; formal analysis: PW-YC, A-YT, and MO; investigation: A-YT; PW-YC; M.O.; resources: A-YT and W-CC; data curation: A-YT; Writing—Original draft preparation: A-YT; PW-YC; Writing—Review and editing: A-YT and VM; funding acquisition: A-YT; VM; W-CC. All authors have read and agreed to the published version of the manuscript. All authors read and approved the final manuscript.
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Chen, P.WY., Olivia, M., Chou, WC. et al. Differences in viral decay and production following exposure to sunlight and dark. Terr Atmos Ocean Sci 34, 8 (2023). https://doi.org/10.1007/s44195-023-00038-2
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DOI: https://doi.org/10.1007/s44195-023-00038-2