Singlet oxygen, a neglected but important environmental factor: short‐term and long‐term effects on bacterioplankton composition in a humic lake

Abstract

Photolysis of dissolved organic matter (DOM) leads to contrasting effects on bacterioplankton dynamics, i.e. stimulation and inhibition of bacterial activity. In particular, the role of short-lived reactive oxygen species (ROS), e.g. singlet oxygen (¹O₂), in altering microbial activity and species composition has scarcely been investigated. Therefore, we have artificially increased the natural rate of ¹O₂ formation in short-term (∼4 h) in situ and long-term (72 h) laboratory incubations of surface water samples from a humic acid-rich lake. Denaturing gradient gel electrophoresis (DGGE) patterns revealed significant changes in occurrence of abundant bacterioplankton phylotypes upon ¹O₂ exposure. Cluster analysis of DGGE patterns showed that a moderate increase in ¹O₂ exposure leads to similar changes in different years indicating the establishment of bacterial communities adapted to ¹O₂ exposure. Bacterioplankton phylotypes favoured under these conditions belonged to Betaproteobacteria of the beta II cluster (e.g. Polynucleobacter necessarius) and the beta I cluster related to Limnohabitans (R-BT subcluster) as well as Alphaproteobacteria affiliated to Novosphingobium acidiphilum. In contrast, Actinobacteria of the freshwater acI-B cluster were sensitive even against moderate ¹O₂ exposure. We conclude that ¹O₂ exposure due to DOM photolysis represents an important natural selective factor affecting bacterial species dynamics in aquatic ecosystems in many ways.

Surface exposure to sunlight stimulates CO2release from permafrost soil carbon in the Arctic

“…3). Because shifts in bacterial community composition are related to the degree of change in bacterial substrates (29), these results support the idea that photobleaching and quantum yield of stimulated bacterial production are proxies for total photochemical transformations of DOM; increased photo-transformation alters DOM chemistry relative to the dark control, which in turn drives and supports shifts in bacterial species and activity. This result also suggests that natural bacterial communities in thermokarstdisturbed waters have the genetic and metabolic capacity to process deep soil C when it is exposed to surface conditions.…”

Phosphoprotein SAK1 is a regulator of acclimation to singlet oxygen in Chlamydomonas reinhardtii

“…This was not surprising considering that 1 O 2 exists in aquatic and terrestrial environments, where it is generated by photosensitizing humic substances (Frimmel et al, 1987; Steinberg et al, 2008), which are known to affect microbial populations including phytoplankton (Glaeser et al, 2010, 2014). Assuming that some of these transporters function to export photosensitizing molecules from the cell, our results suggest that removal of photosensitizers is an integral part of the 1 O 2 response in Chlamydomonas , rather than simply a response to the presence of a xenobiotic compound such as RB (Table 4).…”

Photodegraded dissolved organic matter from peak freshet river discharge as a substrate for bacterial production in a lake-rich great Arctic delta

“…For example, Febria et al (2006) found that the production of hydrogen peroxide (H 2 O 2 ) in two delta lakes that were also sampled herein (CON and TK) outpaced the rate of removal during a period of uninterrupted sunshine in 2004, leading to an accumulation of H 2 O 2 within the water columns. Production of ROS during previous studies of DOM photodegradation has been observed to inhibit community-level rates of carbon production (Scully et al 2003;Anesio et al 2005;Glaeser et al 2014) and result in changes in bacterial community composition (Glaeser et al 2010(Glaeser et al , 2014. Further, in a prior study by Lund and Hongve (1994), declines in BA of up to 60% were observed after only an hour when UV-irradiated DOM was mixed with bacteria.…”

“…To some extent, therefore, irradiation of DOM by sunlight simultaneously stimulates and inhibits heterotrophic bacterial production (BP) (Scully et al 2003;Ruiz-Gonzalez et al 2013), leading to complex interactions that can result in enhanced, negative, mixed, or no effect on bacterial community metabolism (Lonborg et al 2016). In addition, the bacterial community composition may be altered either by exposure to ROS (Glaeser et al 2010;Glaeser et al 2014) or in response to the increased lability of the pool of DOM substrate (Judd et al 2007;Piccini et al 2009;Paul et al 2012;Ward et al 2017), giving rise to a species assemblage that is better suited to the ambient conditions.…”