Doctoral Dissertations

Date of Award

8-2013

Degree Type

Dissertation

Degree Name

Doctor of Philosophy

Major

Microbiology

Major Professor

Alison Buchan

Committee Members

Steven W. Wilhelm, Erik R. Zinser, John Sanseverino, Jennifer M. DeBruyn

Abstract

Roseobacters are an abundant and trophically versatile lineage of marine bacteria that are especially dominant in coastal salt marshes. Central to understanding of how members of the Roseobacter clade contribute to biogeochemical cycling in the world’s oceans is how these bacteria physiologically respond to mixtures of usable growth substrates present in their environmental niches. A prior study provided evidence that bacterioplankton transcripts most closely related to the Roseobacter Sagitulla stellata E-37 are among the most abundant in coastal systems for biogeochemically significant processes of N, P, and S cycling. Thus, this strain was used throughout this dissertation as an environmentally relevant model. Most roseobacter isolates contain multiple aerobic ring-cleaving pathways for the degradation of aromatic compounds, yet it was unknown whether cross-regulation occurred between different parallel pathways. In S. stellata E-37, benzoate is catabolized through the aerobic benzoyl-CoA oxidation (box) pathway, and p-hydroxybenzoate proceeds through the protocatechuate (pca) branch of the beta-ketoadipate pathway. Temporal analysis of S. stellata E-37 was performed in a mixed-substrate environment containing both benzoate and p-hydroxybenzoate and showed that both substrates were simultaneously catabolized at the same rate. Computational and further experimental studies suggest this phenotype appears unique to roseobacters and is anticipated to confer an ecological growth advantage. Additional studies focusing on the environmental relevance of the box pathway revealed it is an abundant yet taxonomically constrained pathway to Betaproteobacteria and Roseobacter. Finally, a study was performed to examine the response of S. stellata E-37 to a more chemically complex environment. In coastal salt marshes where roseobacters are dominant, Spartina alterniflora (cordgrass) is the most abundant primary producer and Phaeosphaeria spartinicola is an abundant and active lignocellulose-degrading fungus. Cordgrass degradation products (mediated by P. spartinicola), representing a salt marsh-like dissolved organic carbon (DOC) mixture, were provided to S. stellata E-37 to link metabolic processes to mineralization of cordgrass. Multiple ring-cleaving and carbohydrate metabolism genes were induced during growth on the DOC mixture. Furthermore, the overexpression of central metabolism pathways such as the tricarboxylic acid (TCA) cycle, ATPase, and NADH dehydrogenase suggest a hyperactive trophic strategy for this metabolically versatile roseobacter.

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