Beach sand oil spills select for generalist microbial populations

Patrick Heritier-Robbins,Markus Huettel,Konstantinos T Konstantinidis,Minjae Kim,Smruthi Karthikeyan,Luis M Rodriguez-R,Joel E Kostka,Janet K Hatt

doi:10.1038/s41396-021-01017-6

Abstract

The specialization-disturbance hypothesis predicts that, in the event of a disturbance, generalists are favored, while specialists are selected against. This hypothesis has not been rigorously tested in microbial systems and it remains unclear to what extent it could explain microbial community succession patterns following perturbations. Previous field observations of Pensacola Beach sands that were impacted by the Deepwater Horizon (DWH) oil spill provided evidence in support of the specialization-disturbance hypothesis. However, ecological drift as well as uncounted environmental fluctuations (e.g., storms) could not be ruled out as confounding factors driving these field results. In this study, the specialization-disturbance hypothesis was tested on beach sands, disturbed by DWH crude oil, ex situ in closed laboratory advective-flow chambers that mimic in situ conditions in saturated beach sediments. The chambers were inoculated with weathered DWH oil and unamended chambers served as controls. The time series of shotgun metagenomic and 16S rRNA gene amplicon sequence data from a two-month long incubation showed that functional diversity significantly increased while taxonomic diversity significantly declined, indicating a decrease in specialist taxa. Thus, results from this laboratory study corroborate field observations, providing verification that the specialization-disturbance hypothesis can explain microbial succession patterns in crude oil impacted beach sands.

Highlights

We recently presented support for the specializationdisturbance hypothesis when we showed that reduced taxonomic diversity coupled to increased functional diversity characterized the response of sedimentary microbial communities from Pensacola Beach (Florida, USA) to the Deepwater Horizon (DWH) crude oil spill [7]
Generalist taxa were defined as operational taxonomic units (OTU) having broad niche breadth reflected by increased number of non-redundant protein functions, whereas specialist taxa were defined as OTUs having a narrow niche breadth characterized by fewer nonredundant protein functions
A tool that estimates what fraction of the microbial community is represented in a metagenome by examining the level of redundancy among the metagenomic reads [13], showed that coverage of the sampled microbial communities by sequencing was adequate for comparison [14], with 60–75% sample coverage for oiled mesocosm and 45–70% for control sample

Summary

Introduction

The specialization-disturbance hypothesis, coined by Vázquez and Simberloff [1], predicts that disturbances negatively affect specialists while benefiting generalists. This is because specialist taxa are adapted to narrow niches, and are selected against when disturbance transforms their environment outside of their niche boundaries. Disturbed communities are often observed to encompass reduced taxonomic and/or phylogenetic diversity compared with undisturbed controls, but whether this pattern translates to increased functional diversity remains largely unknown. We recently presented support for the specializationdisturbance hypothesis when we showed that reduced taxonomic diversity coupled to increased functional diversity characterized the response of sedimentary microbial communities from Pensacola Beach (Florida, USA) to the Deepwater Horizon (DWH) crude oil spill [7].

C Pensacola Field

Results and discussion

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