Species-specific responses of marine bacteria to environmental perturbation

Tito D Peña-Montenegro; Sara Kleindienst; Andrew E Allen; A Murat Eren; John P McCrow; Juan D Sánchez-Calderón; Jonathan Arnold; Samantha B Joye

doi:10.1038/s43705-023-00310-z

Species-specific responses of marine bacteria to environmental perturbation

ISME Commun. 2023 Sep 22;3(1):99. doi: 10.1038/s43705-023-00310-z.

Authors

Tito D Peña-Montenegro^{1

2

3}, Sara Kleindienst^{1

4}, Andrew E Allen^{5

6}, A Murat Eren^{7

8}, John P McCrow⁵, Juan D Sánchez-Calderón⁹, Jonathan Arnold^{2

10}, Samantha B Joye¹¹

Affiliations

¹ Department of Marine Sciences, University of Georgia, 325 Sanford Dr., Athens, GA, 30602-3636, USA.
² Institute of Bioinformatics, University of Georgia, 120 Green St., Athens, GA, 30602-7229, USA.
³ Grupo de Investigación y Desarrollo en Ciencias, Tecnología e Innovación (BioGRID), Sociedad de Doctores e Investigadores de Colombia (SoPhIC), Bogotá, Colombia.
⁴ Department of Environmental Microbiology, Institute for Sanitary Engineering, Water Quality and Solid Waste Management (ISWA), University of Stuttgart, Bandtäle 2, 70569, Stuttgart, Germany.
⁵ Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA, 92037, USA.
⁶ Integrative Oceanography Division, Scripps Institution of Oceanography, UC San Diego, La Jolla, CA, 92037, USA.
⁷ Helmholtz Institute for Functional Marine Biodiversity at the University of Oldenburg, University of Oldenburg, Oldenburg, 26129, Germany.
⁸ Josephine Bay Paul Center, Marine Biological Laboratory, Woods Hole, MA, USA.
⁹ Grupo de Investigación en Gestión Ecológica y Agroindustrial (GEA), Programa de Microbiología, Facultad de Ciencias Exactas y Naturales, Universidad Libre, Seccional Barranquilla, Barranquilla, Colombia.
¹⁰ Department of Genetics, University of Georgia, 120 Green St., Athens, GA, 30602-7223, USA.
¹¹ Department of Marine Sciences, University of Georgia, 325 Sanford Dr., Athens, GA, 30602-3636, USA. mjoye@uga.edu.

Abstract

Environmental perturbations shape the structure and function of microbial communities. Oil spills are a major perturbation and resolving spills often requires active measures like dispersant application that can exacerbate the initial disturbance. Species-specific responses of microorganisms to oil and dispersant exposure during such perturbations remain largely unknown. We merged metatranscriptomic libraries with pangenomes to generate Core-Accessory Metatranscriptomes (CA-Metatranscriptomes) for two microbial hydrocarbon degraders that played important roles in the aftermath of the Deepwater Horizon oil spill. The Colwellia CA-Metatranscriptome illustrated pronounced dispersant-driven acceleration of core (~41%) and accessory gene (~59%) transcription, suggesting an opportunistic strategy. Marinobacter responded to oil exposure by expressing mainly accessory genes (~93%), suggesting an effective hydrocarbon-degrading lifestyle. The CA-Metatranscriptome approach offers a robust way to identify the underlying mechanisms of key microbial functions and highlights differences of specialist-vs-opportunistic responses to environmental disturbance.

Abstract

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