A total of 62 samples from 31 stations were collected from the surface water of the Bohai Sea in winter 2013 and summer 2014. The maximum, minimum, median, mean and standard deviation (SD) of the measured environmental variables from winter and summer are presented in Table 1. The surface water temperature in winter ranged from 3.2°C to 9.95°C (Fig. 3, Table 1), and it presented an obvious decreasing trend from the east to the west of the Bohai Sea. In summer, the highest temperature was 26.26°C, and the lowest temperature was 19.71°C. We found that the temperature was lowest on the northern side of the Bohai Strait throughout the total study area (Fig. 3, Table 1). Compared with temperature, the range of salinity in winter and in summer did not vary much (maximum and minimum salinity in winter were 32.95 and 29.11, respectively; maximum and minimum salinity in summer were 31.31 and 29.32, respectively) (Fig. 3, Table 1). The results showed that the area of high salinity in winter and summer was located near the north and east of the Bohai Strait.
Season Temperature/°C Salinity NO2-N/µg·L−1 NO3-N/µg·L−1 NH4-N/µg·L−1 PO4-P/µg·L−1 SiO2/µg·L−1 Winter Max 9.95 33.15 37.1 669.0 166.9 69.2 2.46 Min 3.20 29.11 1.7 1.0 10.3 0.3 0.14 Mean 6.69 31.19 7.6 224.8 68.7 8.2 0.67 SD 2.01 0.89 6.5 195.0 40.8 15.3 0.65 Summer Max 26.26 31.31 38.16 201.5 70.8 9.3 0.62 Min 19.71 28.93 0.27 1.7 0.5 0.67 0.06 Mean 24.16 30.29 5.81 40.33 15.87 3.20 0.26 SD 1.75 0.53 9.41 47.57 13.98 2.07 0.15
Table 1. Summary of environmental parameters from surface water of the Bohai Sea in winter 2013 and summer 2014
Figure 3. Distributions of temperature and salinity in the surface water of the Bohai Sea (winter 2013 and summer 2014).
The distributions of the dissolved inorganic matter (NO3-N, NO2-N, NH4-N, PO4-P and SiO2) in winter and summer in the Bohai Sea are shown in Fig. 4. The concentrations of nutrients at stations located in the middle of the Bohai Sea were much higher than those in the other areas. The high concentration distribution of NO2-N, NH4-N and PO4-P was consistently observed in summer. However, the concentrations of NO3-N and SiO2 appeared to be high in the west of the Bohai Sea (Fig. 4). In winter and summer, there were great discrepancies in the distribution of dissolved nutrient factors.
In winter 2013, the total viral abundance ranged from 1.87×107 to 1.10×109 particles/mL in the surface water. In summer 2014, the total viral abundance of the surface water ranged from 1.06×106 to 2.54×109 particles/mL. The average measured abundance of total virus in winter and summer was 2.29×108 particles/mL and 3.83×108 particles/mL respectively (Fig. 5). In view of the average viral abundance, there was no significant difference between the two seasons. However, for the distribution, a high abundance area appeared in the east of the Bohai Sea in winter and in the middle of the Bohai Strait in summer.
Figure 5. Total virus and total bacteria abundance in the surface water of Bohai Sea (winter 2013 and summer 2014). TV represents total virus abundance and TB total bacteria abundance.
In regard to two viral populations (Figs 2, 6 and 7a), VLP1 and VLP2 were observed to be present at all stations in winter and summer in the Bohai Sea. The average abundances of VLP1 in winter were much lower than the abundances in summer. Along all stations of surface water in the Bohai Sea, the abundances of VLP1 and VLP2 in winter ranged from 1.27×107 to 6.23×108 particles/mL and 5.10×106 to 4.84×108 particles/mL, respectively. In summer, the abundance of VLP1 and VLP2 ranged from 2.26×105 to 1.87×109 particles/mL and 8.02×105 to 6.67×108 particles/mL, respectively.
Figure 6. Community abundances of virus and bacteria in the surface water of the Bohai Sea. V1: bacteriophage, VLP1; V2: cyanophages, VLP2; B1: LDNA; B2: HDNA1; and B3: HDNA2.
Figure 7. Comparison of virioplankton and bacterioplankton abundance in winter and summer. a. Average abundance of VLP1 and VLP2 in winter and summer; b. average abundance of LDNA, HDNA1 and HDNA2 in winter and summer; and c. histogram used to describe the average abundance of VLP1, VLP2, LDNA, HDNA1, HDNA2, TV and TB in winter and summer. TV represents total virus abundance, TB total bacteria abundance, VLP1 virus-like particle 1, VLP2 virus-like particle 2, HDNA1 high DNA bacteria 1, HDNA2 high DNA bactria 2, and LDNA low DNA bacteria.
VLP1 dominated the composition of the total viral community and represented up to 52% of the total abundance in surface water of winter (Figs 7a-c). The highest abundance of VLP1 in winter was observed at Stations L2, K6 and R7. In summer, VLP1 dominated the composition of the total viral community up to approximately 73%. The highest abundance of VLP1 appeared at Stations E3, E4 and L5 (Fig. 6).
The total bacterial abundance ranged from 1.02×106 to 1.38×108 particles/mL in winter and ranged from 6.74×105 to 4.24×108 particles/mL in summer. The average abundances of bacteria in winter and summer were 2.54×107 and 5.43×107 particles/mL, respectively. The total bacterial abundance of summer was apparently much higher than the abundance of winter. Meanwhile, a high abundance area could be found at Stations K2 and L2 in winter. In summer, there was a significant increase in the abundance of some stations such as E6 and N5 (Fig. 5).
The bacterial community could be divided into three groups, which included one low LDNA population and two high HDNA populations (HDNA1 and HDNA2), by observing the entire station (Figs 2 and 7b). The highest abundance of LDNA was found at K6 in winter and N5 in summer. In the surface water of the Bohai Sea, the total abundance of bacteria in summer was much higher than that in winter. The abundance of HDNA2 accounted for the smallest portion in both winter and summer, but it presented a significant increase in summer, which resulted in a high abundance of the total bacteria (P<0.05) (Fig. 7b). This pattern is because that the increase in the HDNA2 population causes the higher total abundance of bacteria in summer than that in winter. Therefore, the average virus-to-bacteria ratio (VBR) is much lower in summer (5.72) than that in winter (13.72).
To analyze the bacterial community composition, we measured that the average abundance of HDNA1 in winter accounted for 48% of the total bacterial abundance, and in summer, this proportion was approximately 38% (Fig. 7c). In the surface water of the Bohai Sea, the abundance of LDNA was the most abundant community whether it is in winter or in summer (Figs 7b, c).
We used RDA and network correlation analysis to assess the relationships among virioplankton populations, bacterioplankton populations and environmental factors in winter and summer in the Bohai Sea. According to the results of RDA, stations near the eastern part of the Bohai Sea presented a close relationship with temperature in winter, and transects near the Bohai Strait had a close connection with salinity in summer. There was a significant positive relationship among temperature and LDNA, HDNA1, HDNA2, and total bacteria in winter (Figs 8a and 9). Meanwhile, in summer, there was a positive relationship among salinity and VLP1, VLP2, total virus and VBR, and there was a significant negative relationship among salinity and SiO2 and LDNA, HDNA1, HDNA2 and total bacteria (Figs 8b and 9). According to network analysis, we verified the results of RDA. We found that HDNA2 had a positive correlation with temperature and salinity in winter. There was a significant positive correlation between the NO3-N+NO2-N, NO3-N and VBR values in winter. Meanwhile, there was a significant negative correlation between VBR and NO2-N, temperature and salinity. In summer, salinity was a positive correlation factor that controlled the VLP1 and VBR values. SiO2, PO4-P and temperature had a significant negative correlation effect on the abundances of virioplankton and bacterioplankton (Fig. 9).
Figure 8. RDA analyze of the viral, bacterial groups and environmental factors in the surface water of the Bohai Sea. a. Winter in 2013 and b. summer in 2014. VBR represents virus to bacteria ratio, Tem temperature, Sal salinity, Nitrite NO2-N, Nitrate NO3-N, Ammo NH4-N, Phos PO4-P, Sili SiO2, and ○ stations in the Bohai Sea.
Figure 9. Network analysis for the correlation between total viral abundance (TV), total bacteria abundance (TB), VLP1 (V1), VLP2 (V2), LDNA (B1), HDNA1 (B2), HDNA2 (B3) and environmental factors which include temperature, salinity, NO3-N+NO2-N, NO2-N, NO3-N, NH4-N, PO4-P and SiO2. a and b. The positive and negative relationships in winter, respectively; and c and d. the positive and negative relationships in summer, respectively. The blue nodes represent the environmental factors. Edge with width of 4 represent that there are significant correlations between different populations and environmental variables (p<0.01). Edge with width of 2 represent that there are significant correlations between different populations and environmental variables (p<0.05). Edge with width of 0.1 represent that there are no significant relationships between different populations and environmental variables.
Coupling virio- and bacterioplankton populations with environmental variable changes in the Bohai Sea
- Received Date: 2019-07-02
- Accepted Date: 2019-09-25
- Available Online: 2020-12-28
- Publish Date: 2020-06-25
Abstract: Uncovering the role of environmental factors and finding critical factors which harbor significant fractions in governing microbial communities remain key questions in coastal marine systems. To detect the interactions between environmental factors and distributions of virio- and bacterioplankton in trophic coastal areas, we used flow cytometry to investigate the abundance of virio- and bacterioplankton covering 31 stations in the Bohai Sea of China. Our results suggested that the average abundance of total virus (TV) in winter (~2.29×108 particles/mL) was slightly lower than in summer (~3.83×108 particles/mL). The mean total bacterial abundance (TB) was much lower in winter (~2.54×107 particles/mL) than in summer (~5.43×107 particles/mL). Correlation analysis via redundancy analysis (RDA) and network analysis among virioplankton, bacterioplankton and environmental factors revealed that the abundances of viral and bacterial subpopulations depend on environmental factors. In winter, only temperature significantly influenced the abundances of virio- and bacterioplankton. In summer, in addition to temperature, both salinity and nutrient (SiO2) had a remarkable impact on the distribution of virio- and bacterioplankton. Our results showed a clear seasonal and trophic pattern throughout the whole water system, which revealed that temperature and eutrophication may play crucial roles in microbial distribution pattern.
|Citation:||Caixia Wang, Lin Wu, Yibo Wang, James S. Paterson, James G. Mitchell, Xiaoke Hu. Coupling virio- and bacterioplankton populations with environmental variable changes in the Bohai Sea[J]. Acta Oceanologica Sinica, 2020, 39(6): 72-83. doi: 10.1007/s13131-020-1591-3|