Microbial responses to anthropogenic dissolved organic carbon in the Arctic and Antarctic coastal seawaters

Abstract

Summary Thousands of semi‐volatile hydrophobic organic pollutants (OPs) reach open oceans through atmospheric deposition, causing a chronic and ubiquitous pollution by anthropogenic dissolved organic carbon (ADOC). Hydrophobic ADOC accumulates in cellular lipids, inducing harmful effects on marine biota, and can be partially prone to microbial degradation. Unfortunately, their possible effects on microorganisms, key drivers of global biogeochemical cycles, remain unknown. We challenged coastal microbial communities from Ny‐Ålesund (Arctic) and Livingston Island (Antarctica) with ADOC concentrations within the range of oceanic concentrations in 24 h. ADOC addition elicited clear transcriptional responses in multiple microbial heterotrophic metabolisms in ubiquitous groups such as Flavobacteriia, Gammaproteobacteria and SAR11. Importantly, a suite of cellular adaptations and detoxifying mechanisms, including remodelling of membrane lipids and transporters, was detected. ADOC exposure also changed the composition of microbial communities, through stimulation of rare biosphere taxa. Many of these taxa belong to recognized OPs degraders. This work shows that ADOC at environmentally relevant concentrations substantially influences marine microbial communities. Given that emissions of organic pollutants are growing during the Anthropocene, the results shown here suggest an increasing influence of ADOC on the structure of microbial communities and the biogeochemical cycles regulated by marine microbes.

Large Enrichment of Anthropogenic Organic Matter Degrading Bacteria in the Sea-Surface Microlayer at Coastal Livingston Island (Antarctica)

“…Colwellia, Pseudomonas, and Pseudoalteromanas are generalist strains with rapid facultative degrading capabilities toward ADOC, but also prompt to degrade other dissolved organic matter compounds. Colwellia have been described as abundant and fast responder following ADOC background concentration exposures in polar environments (Cerro-Gálvez et al, 2019), and to oil spills in marine environments (Gutierrez et al, 2013;Dombrowski et al, 2016;Lofthus et al, 2018;Vergeynst et al, 2018). In fact, Colwellia single cell assembled genomes (SAGs) retrieved from contaminated marine sites have revealed a more specific metabolic activity toward aromatic hydrocarbons, as well as a full set of genes involved with chemotaxis, motility and adaptations to cold environments such as Antarctica (Mason et al, 2014).…”

Direct effects of organic pollutants on the growth and gene expression of the Baltic Sea model bacteriumRheinheimerasp.BAL341

“…Generally, the gene expression responses were detected in a variety of categories of gene functions (recorded both as number of genes influenced in different categories and as their relative expression levels), indicating that the studied OPs had a broad impact on bacterial physiology. Moreover, as much as 85% of the significantly differentially expressed genes were unique for each pollutant treatment, suggesting a high degree of pollutant‐specific physiological responses in marine bacteria (Cerro‐Galvez et al ., ).…”

“…It is widely recognized that toxic OPs accumulate in food chains due to their hydrophobicity, and the effects of specific pollutants on higher marine life are extensively studied (Hylland, ; Schwarzenbach et al ., ; Keyte et al ., ; Harmon, ). However, knowledge of the effects on microorganisms of the myriad of OPs (including POPs and SOCs) circulating in the marine environment remains scarce (Dachs and Méjanelle, ; Cerro‐Galvez et al ., ).…”

“…Hydrocarbons in the marine environment can stimulate the growth rates of bacteria and also select for specific bacterial groups (for example members of the genera Cycloclasticus , Marinobacter , Oceanospirillum ) (Zobell, ; Leahy and Colwell, ; Teira et al ., ; Seo et al ., ; Rivers et al ., ). Broadly considered, OPs can influence microorganisms by stimulating growth (acting as a food source) or by negatively affecting growth as a result of toxicological effects (Singh and Walker, ; Echeveste et al ., ; Duran and Cravo‐Laureau, ; Fernandez‐Pinos et al ., ; Cerro‐Galvez et al ., ; Vila‐Costa et al ., ). Recent research has used advanced molecular methods to identify the mechanisms used by natural bacterial communities to degrade toxic linear or branched hydrocarbons (alkanes) and PAH from oil spill events (Rivers et al ., ; Wang et al ., ; Handley et al ., ).…”

The Link Between the Ecology of the Prokaryotic Rare Biosphere and Its Biotechnological Potential

“…In another study, Giebler et al (2013) identified a possible seed bank of rare prokaryotes, originated from pristine soils, with the ability to degrade alkanes. Finally, manipulative experiments with Arctic and Antarctic microplankton communities showed that the addition of hydrophobic, anthropogenic dissolved organic carbon reduced overall microbial diversity and that the degradation response was mediated by rare prokaryotes (Cerro-Gálvez et al, 2019).…”