Virus-bacterium coupling driven by both turbidity and hydrodynamics in an Amazonian floodplain lake

Abstract

The importance of viruses in aquatic ecosystem functioning has been widely described. However, few studies have examined tropical aquatic ecosystems. Here, we evaluated for the first time viruses and their relationship with other planktonic communities in an Amazonian freshwater ecosystem. Coupling between viruses and bacteria was studied, focusing both on hydrologic dynamics and anthropogenic forced turbidity in the system (Lake Batata). Samples were taken during four hydrologic seasons at both natural and impacted sites to count virus-like particles (VLP) and bacteria. In parallel, virus-infected bacteria were identified and quantified by transmission electron microscopy (TEM). Viral abundance ranged from 0.5 × 10⁷ ± 0.2 × 10⁷ VLP ml⁻¹ (high-water season, impacted site) to 1.7 × 10⁷ ± 0.4 × 10⁷ VLP ml⁻¹ (low-water season, natural site). These data were strongly correlated with the bacterial abundance (r² = 0.84; P < 0.05), which ranged from 1.0 × 10⁶ ± 0.5 × 10⁶ cells ml⁻¹ (high water, impacted site) to 3.4 × 10⁶ ± 0.7 × 10⁶ cells ml⁻¹ (low water, natural site). Moreover, the viral abundance was weakly correlated with chlorophyll a, suggesting that most viruses were bacteriophages. TEM quantitative analyses revealed that the frequency of visibly infected cells was 20%, with 10 ± 3 phages per cell section. In general, we found a low virus-bacterium ratio (<7). Both the close coupling between the viral and bacterial abundances and the low virus-bacterium ratio suggest that viral abundance tends to be driven by the reduction of hosts for viral infection. Our results demonstrate that viruses are controlled by biological substrates, whereas in addition to grazing, bacteria are regulated by physical processes caused by turbidity, which affect underwater light distribution and dissolved organic carbon availability.

FIG. 1.

Map of the Amazon watershed and the location of Lake Batata, the sampling site.

FIG. 2.

Virus abundance (A), bacterial abundance (B), and virus-bacterium ratio (C) at the impacted (black bars) and natural (white bars) sites in different seasons of the flood pulse. FL, filling; HW, high water; D, drawdown; LW, low water. Bars and traces represent means and standard deviations, respectively.

FIG. 3.

Simple linear regression analysis between viral and bacterial abundances. Black and white points represent the impacted and natural sites, respectively. Lines around the points are standard errors, and the dashed lines represent 95% confidence interval for the linear regression.

FIG. 4.

Electron micrographs of bacteria from Lake Batata. (A and B) Uninfected bacteria. Bacterial structures such as cytoplasm (c), nucleoid (n), periplasmic space (*), and external capsule (arrowheads) are clearly observed. (A) Two morphologically distinct types of bacteria are seen in the same field. Note the variable thickness of the bacterial capsule, which is thicker and denser in panel A (arrowheads) than in panel B (arrowheads.) The boxed area in panel B is shown at a higher magnification at the bottom of the same figure. Note the strongly electron-dense cell wall below the capsule (arrowheads). (C) Virus-infected bacterium with several phages. The boxed area shows the virus capsid structure at high magnification. Note that the capsid is composed of repetitive morphological units (highlighted in blue at a higher magnification). The cell membrane is partially observed (arrows). Scale bars, 460 nm (A and B), 300 nm (B, high magnification), 266 nm (C), 80 nm (C, virus at high magnification), and 40 nm (C, virus at higher magnification, highlighted in blue).