Away from darkness: a review on the effects of solar radiation on heterotrophic bacterioplankton activity

Abstract

Heterotrophic bacterioplankton are main consumers of dissolved organic matter (OM) in aquatic ecosystems, including the sunlit upper layers of the ocean and freshwater bodies. Their well-known sensitivity to ultraviolet radiation (UVR), together with some recently discovered mechanisms bacteria have evolved to benefit from photosynthetically available radiation (PAR), suggest that natural sunlight plays a relevant, yet difficult to predict role in modulating bacterial biogeochemical functions in aquatic ecosystems. Three decades of experimental work assessing the effects of sunlight on natural bacterial heterotrophic activity reveal responses ranging from high stimulation to total inhibition. In this review, we compile the existing studies on the topic and discuss the potential causes underlying these contrasting results, with special emphasis on the largely overlooked influences of the community composition and the previous light exposure conditions, as well as the different temporal and spatial scales at which exposure to solar radiation fluctuates. These intricate sunlight-bacteria interactions have implications for our understanding of carbon fluxes in aquatic systems, yet further research is necessary before we can accurately evaluate or predict the consequences of increasing surface UVR levels associated with global change.

Keywords: aquatic ecosystems; bacterial heterotrophic activity; bacterioplankton community composition; light history; solar radiation.

Figure 1

Positive and negative effects of natural or simulated solar radiation on marine bacterial activity in natural samples. Range of reported light-driven effects on bacterial heterotrophic activity from different marine systems measured as (A) ³H-leucine or (B) ³H-thymidine incorporation rates and expressed as the ratio to dark incubation rates. Whether samples were exposed to natural or simulated radiation (PAR or UVB lamps) is also indicated. Note the logarithmic scales of the ratio on the Y axes. Data were extracted from 31 marine studies in which a dark control was available for comparison with light treatments. Experiments where something else than light was manipulated (e.g., nutrients or temperature) were not considered. (1) Carlucci et al., ; (2) Aas et al., ; (3) Sommaruga et al., ; (4) Visser et al., ; (5) Morán et al., ; (6) Church et al., ; (7) Alonso-Sáez et al., ; (8) Church et al., ; (9) Hernández et al., ; (10) Michelou et al., ; (11) Pakulski et al., ; (12) Calvo-Díaz, ; (13) Joux et al., ; (14) Bertoni et al., ; (15) del Valle et al., ; (16) Ruiz-González et al., ; (17) Ruiz-González et al., ; (18) Ruiz-González et al., ; (19) Herndl et al., ; (20) Pakulski et al., ; (21) Ruiz-González et al., ; (22) Kaiser and Herndl, ; (23) Pakulski et al., ; (24) Chróst and Faust, ; (25) Visser et al., ; (26) Bullock and Jeffrey, ; (27) Shiah, ; (28) Renaud et al., ; (29) Conan et al., ; (30) Rochelle-Newall et al., ; (31) Müller-Niklas et al., .

Figure 2

Positive and negative effects of natural or simulated solar radiation on freshwater and estuarine bacterial activity in natural samples. Range of reported light-driven effects on bacterial heterotrophic activity from different freshwater and estuarine systems measured as (A) ³H-leucine or (B) ³H-thymidine incorporation rates and expressed as the ratio to dark incubation rates. Whether samples were exposed to natural or simulated radiation (visible light or UVB lamps) is also indicated. Data extracted from 12 freshwater or estuarine studies in which a dark control was available for comparison with light treatments. Experiments where something else than light was manipulated (e.g., nutrients or temperature) were not considered. Note the logarithmic scales of the ratio on the Y axes. (1) Aas et al., ; (2) Sommaruga et al., ; (3) Ziegler and Benner, ; (4) Straza and Kirchman, ; (5) Amon and Benner, ; (6) Lindell and Edling, ; (7) Bullock and Jeffrey, ; (8) Santos et al., ; (9) Santos et al., ; (10) Carrillo et al., ; (11) Medina-Sánchez et al., ; (12) Medina-Sánchez et al., .

Figure 3

Sunlight-modulated interactions among microbes and molecules. Simplified scheme of the pelagic marine food web illustrating the processes susceptible to be modulated by solar radiation either positively (+) or negatively (−), which may ultimately lead to increases or decreases in the heterotrophic activity of bacterioplankton.

Figure 4

Diverse responses to sunlight spectrum conditions among different bacterial groups. Light-driven effects on the percentage of cells active in ³H-leucine uptake among different bacterial groups as determined by MAR-CARD-FISH in natural samples. Up- and down arrows indicate significant increase or decrease in the proportion of active cells, respectively, caused by PAR (or PAR + UVA in the case of polar samples, yellow arrows) or full sunlight exposure (or UVB in the case of polar samples, blue arrows). Mediterranean data from Alonso-Sáez et al. (2006) and Ruiz-González et al. (2012f); Arctic and Antarctic values from Ruiz-González et al. (2012a).

Figure 5

Trends in responses to sunlight of bacterial groups from distinct habitats. Relationships between sunlight-driven changes in the number of cells active in ³H-leucine uptake caused by full sunlight exposure (expressed as % of a dark control) and the UVB irradiances or the UVA to UVB ratio received by the samples in two subgroups of Alphaproteobacteria: the SAR11 clade (A,B) and Roseobacter (C,D). Mediterranean data from Alonso-Sáez et al. (2006) and Ruiz-González et al. (2012f); Arctic and Antarctic values from Ruiz-González et al. (2012a).

Figure 6

Effects of PAR (natural or simulated) on the uptake of various radiolabeled organic substrates by different bacterioplankton groups as identified by MAR-CARD-FISH or flow cytometry cell sorting. Arrows indicate whether PAR-stimulation, inhibition, or no effects were observed in various experiments done in the Sargasso Sea and the North Carolina (NC) coast (Malmstrom et al., 2005), the North Atlantic (Michelou et al., ; Gómez-Pereira et al., 2013), the Central Atlantic (Mary et al., 2008a), the Delaware Bay (Straza and Kirchman, 2011), and the NW Mediterranean (Alonso-Sáez et al., ; Vila-Costa et al., ; Ruiz-González et al., 2012b,e). The PAR-driven effects observed by Alonso-Sáez et al. (2006) and Ruiz-González et al. (2012b) on substrates other than leucine (see Figure 4) are included even though they also tested UVR radiation effects in their experiments.

Figure 7

Dark vs. light bacterial activity measurements. Comparison between bulk ³H-leucine incorporation rates in different light conditions and dark incubations conducted with surface seawater samples (<5 m) from different systems and with the radiotracer added before exposure. Exposure to simulated PAR caused an average 23% stimulation while PAR+UVR led to an average 20% inhibition in comparison to the dark controls (see text). Mediterranean data from Ruiz-González et al. (2012e); Bay of Biscay (Calvo-Díaz, 2008); Delaware Bay (Straza and Kirchman, 2011); N Atlantic (Michelou et al., 2007); E Pacific (Pakulski et al., 2007); Arctic and Antarctica (Ruiz-González et al., and unpublished).