Molecular mechanism of oil induced growth inhibition in diatoms using Thalassiosira pseudonana as the model species

Manoj Kamalanathan,Antonietta Quigg,Noah Claflin,Savannah Mapes,Jessica Hillhouse,Joshua Leleux,David Hala

doi:10.1038/s41598-021-98744-9

Manoj Kamalanathan, Antonietta Quigg + Show 5 more

Open Access

https://doi.org/10.1038/s41598-021-98744-9

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Abstract

The 2010 Deepwater Horizon oil-spill exposed the microbes of Gulf of Mexico to unprecedented amount of oil. Conclusive evidence of the underlying molecular mechanism(s) on the negative effects of oil exposure on certain phytoplankton species such as Thalassiosira pseudonana is still lacking, curtailing our understanding of how oil spills alter community composition. We performed experiments on model diatom T. pseudonana to understand the mechanisms underpinning observed reduced growth and photosynthesis rates during oil exposure. Results show severe impairment to processes upstream of photosynthesis, such as light absorption, with proteins associated with the light harvesting complex damaged while the pigments were unaffected. Proteins associated with photosynthetic electron transport were also damaged, severely affecting photosynthetic apparatus and depriving cells of energy and carbon for growth. Negative growth effects were alleviated when an organic carbon source was provided. Further investigation through proteomics combined with pathway enrichment analysis confirmed the above findings, while highlighting other negatively affected processes such as those associated with ferroxidase complex, high-affinity iron-permease complex, and multiple transmembrane transport. We also show that oxidative stress is not the primary route of negative effects, rather secondary. Overall, this study provides a mechanistic understanding of the cellular damage that occurs during oil exposure to T. pseudonana.

Highlights

The 2010 Deepwater Horizon oil-spill exposed the microbes of Gulf of Mexico to unprecedented amount of oil
Exposure of T. pseudonana to a water accommodated fraction (WAF) of oil resulted in significantly lower cell counts throughout the growth cycle compared to the Control (Fig. 1a)
Further examination of the morphology showed that T. pseudonana had a nearly 1.75 fold increase in height under WAF compared to the Control, and a 1.17 fold increase in radius (Table 1)

Summary

Introduction

The 2010 Deepwater Horizon oil-spill exposed the microbes of Gulf of Mexico to unprecedented amount of oil. Using a combination of traditional laboratory experiments and modern proteomics approach, we sequentially tested the proposed hypotheses which include (1) oil exposure leads to inhibition of silicon uptake and fatty acid s ynthesis[22,23,24,25], (2) oil exposure leads to oxidative stress and intracellular damage[22,23,24,25,36], and (3) PAHs, the biological toxic component of oil, affect the electron transport between photosystem II and I by directly accepting electrons from P SII37,38. The results presented provide direct and detailed mechanistic evidence of how oil exposure affects growth and photosynthesis in T. pseudonana and an explanation of how oil spills could negatively impact diatoms and other sensitive species and alter the phytoplankton community composition

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