The Phytoplankton Taxon-Dependent Oil Response and Its Microbiome: Correlation but Not Causation

Abstract

Phytoplankton strongly interact with their associated bacteria, both attached (PA), and free-living (FL), and bacterial community structures can be specific to phytoplankton species. Similarly, responses to environmental stressors can vary by taxon, as exemplified by observed shifts in phytoplankton community structure from diatoms to phytoflagellates after the Deepwater Horizon (DWH) oil spill. Here, we assess the extent to which associated bacteria influence the phytoplankton taxon-specific oil response by exposing xenic and axenic strains of three phytoplankton species to oil and/or dispersant. The dinoflagellates Amphidinium carterae and Peridinium sociale, and the diatom Skeletonema sp., all harbored significantly distinct bacterial communities that reflected their host oil response. Oil degrading bacteria were detected in both PA and FL communities of the oil resistant dinoflagellates, but their FL bacteria were more efficient in lipid hydrolysis, a proxy for oil degradation capability. Inversely, the growth rate and photosynthetic parameters of the diatom Skeletonema sp. was the most impacted by dispersed oil compared to the dinoflagellates, and oil-degrading bacteria were not significantly associated to its microbiome, even in the dispersed oil treatment. Moreover, the FL bacteria of Skeletonema did not show significant oil degradation. Yet, the lack of consistent significant differences in growth or photosynthetic parameters between the xenic and axenic cultures after oil exposure suggest that, physiologically, the associated bacteria do not modify the phytoplankton oil response. Instead, both oil resistance and phycosphere composition appear to be species-specific characteristics that are not causally linked. This study explores one aspect of what is undoubtedly a complex suite of interactions between phytoplankton and their associated bacteria; future analyses would benefit from studies of genes and metabolites that mediate algal-bacterial exchanges.

Metabolic relationships of uncultured bacteria associated with the microalgae Gambierdiscus

“…This study also showed that algal‐attached communities in seawater are different from bulk particle‐associated communities, indicating that phycosphere communities are specific and distinct from the regional species pool. The Rhodobacteraceae and Flavobacteriaceae reported here are common members of dinoflagellate microbiomes, whereas Planctomycetes are rare or absent in dinoflagellate microbiome sequence sets (Hasegawa et al ., ; Severin and Erdner, ; Sörenson et al ., ). Crenn and colleagues () compared microbiomes of diatoms from cultures and environmental samples, and reported lower diversity in the former.…”

Efficiency of benthic diatom-associated bacteria in the removal of benzo(a)pyrene and fluoranthene

“…2b) and strains growing on crude oil (Table 3) were observed in the bacterial community associated to Nitzschia. This suggests that these associated hydrocarbonoclastic bacteria may enhance biodegradation of PAHs in non-axenic cultures, as previously highlighted (Mishamandani et al, 2016;Thompson et al, 2017Thompson et al, , 2018Severin and Erdner, 2019). The degradation of PAHs by microorganisms depends on their molecular weight, hydrophobicity, and water solubility (Haritash and Kaushik, 2009).…”

“…The presence of oil-and hydrocarbon-degrading bacteria within the phycosphere has been reported for dinoflagellates and diatoms (Gutierrez et al, 2012;Mishamandani et al, 2016;Severin et al, 2016;Thompson et al, 2017Thompson et al, , 2018. These associated bacteria can influence the phytoplankton taxon-specific response to hydrocarbon pollution and oil spills (Severin and Erdner, 2019). Most studies have concerned planktonic microalgae and their associated bacteria, but little is known about the PAH biodegradation potential of microbenthic organisms.…”

Aggregation and Degradation of Dispersants and Oil by Microbial Exopolymers (ADDOMEx): Toward a Synthesis of Processes and Pathways of Marine Oil Snow Formation in Determining the Fate of Hydrocarbons

“…In addition to the above changes in microbial community activity, it was also found that the mucus-like EPS harbored a very distinct community of interacting microbes, with a specific functionality that was different from those persisting in the surrounding seawater (Ziervogel et al, 2012;Arnosti et al, 2015). These eukaryotic microbes and fungi can transform and degrade oil, sometimes in association with bacteria and dispersants including Corexit (Mishamandani et al, 2016;Severin and Erdner, 2019). Thus, marine snow is a hot spot for microbial activity (Azam, 1998;Arnosti et al, 2015;Doyle et al, 2018Doyle et al, , 2020 and serves as a transport vehicle for hydrocarbons to the seafloor as well as the associated microbial communities (Kowalewska and Konat, 1997;Kowalewska, 1999;Ziervogel et al, 2012;Ziervogel et al, 2014Ziervogel et al, , 2016Arnosti et al, 2015).…”