Effect of Humic Substance Photodegradation on Bacterial Growth and Respiration in Lake Water

Abstract

This study addresses how humic substance (HS) chemical composition and photoreactivity affect bacterial growth, respiration, and growth efficiency (BGE) in lake water. Aqueous solutions of HSs from diverse aquatic environments representing different dissolved organic matter sources (autochthonous and allochthonous) were exposed to artificial solar UV radiation. These solutions were added to lake water passed through a 0.7-mpore-size filter (containing grazer-free lake bacteria) followed by dark incubation for 5, 43, and 65 h. For the 5-h incubation, several irradiated HSs inhibited bacterial carbon production (BCP) and this inhibition was highly correlated with H 2 O 2 photoproduction. The H 2 O 2 decayed in the dark, and after 43 h, nearly all irradiated HSs enhanced BCP (average 39% increase relative to nonirradiated controls, standard error ‫؍‬ 7.5%, n ‫؍‬ 16). UV exposure of HSs also increased bacterial respiration (by ϳ18%, standard error ‫؍‬ 5%, n ‫؍‬ 4), but less than BCP, resulting in an average increase in BGE of 32% (standard error ‫؍‬ 10%, n ‫؍‬ 4). Photoenhancement of BCP did not correlate to HS bulk properties (i.e., elemental and chemical composition). However, when the photoenhancement of BCP was normalized to absorbance, several trends with HS origin and extraction method emerged. Absorbance-normalized hydrophilic acid and humic acid samples showed greater enhancement of BCP than hydrophobic acid and fulvic acid samples. Furthermore, absorbancenormalized autochthonous samples showed ϳ10-fold greater enhancement of BCP than allochthonous-dominated samples, indicating that the former are more efficient photoproducers of biological substrates.

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.…”

“…8b), where an initial sharp increase in SBP also suggested that the surviving bacteria were released from a relative shortage of growth substrate. Increased BP and growth have been observed in the presence of irradiated DOM in many freshwater systems (e.g., Anesio et al 2005;Paul et al 2012), including in the circumpolar Arctic (Cory et al 2013;Ward et al 2017), where photochemical oxidation of DOM accounts for the majority of C processing (Cory et al 2014). Prior work in the Mackenzie Delta has shown that lower molecular weight DOM derived from macrophytes supports higher rates of BGE in communities isolated from a variety of habitats (including TK and CON lakes;Tank 2009).…”

“…Wavelengths in the UV range damage bacterial DNA (Karentz et al 1994) and inhibit BP (Jeffrey et al 1996;Anesio et al 2005;Ruiz-Gonzalez et al 2013) in natural sunlit environments, and these effects may be even more pronounced at high latitudes that experience uninterrupted daylight during the summer solstice. Under natural conditions, we would likely have observed lower rates of BP and growth efficiency due to these direct UV effects.…”

“…In contrast to the positive effects of increased substrate availability on bacterial metabolism, photodegradation also exerts indirect negative effects on aquatic bacteria through the production of free radicals and reactive oxygen species (ROS) (e.g., singlet oxygen, peroxides, and superoxides) (Scully et al 1996). These by-products of the photodegradation process are short-lived, but nevertheless inhibit bacterial growth and production (Lund and Hongve 1994;Henle and Linn 1997;Anesio et al 2005). 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).…”

Depth-dependent molecular composition and photo-reactivity of dissolved organic matter in a boreal lake under winter and summer conditions

“…It has been shown that the combination of initial photochemical degradation of the DOM form smaller molecules and that they are more accessible to microbial degradation. This is also important for the total OM mineralization (Bertilsson and Allard, 1996;Tranvik and Bertilsson, 2001;Anesio et al, 2005). When expanding these findings from short-term incubations over time and space, large seasonal differences in lake OM cycling should be expected in stratified and ice-covered systems where different proportions of the OM are exposed to light during different seasons.…”