Simultaneous Catabolism of Plant-Derived Aromatic Compounds Results in Enhanced Growth for Members of the Roseobacter Lineage

Abstract

Plant-derived aromatic compounds are important components of the dissolved organic carbon pool in coastal salt marshes, and their mineralization by resident bacteria contributes to carbon cycling in these systems. Members of the roseobacter lineage of marine bacteria are abundant in coastal salt marshes, and several characterized strains, including Sagittula stellata E-37, utilize aromatic compounds as primary growth substrates. The genome sequence of S. stellata contains multiple, potentially competing, aerobic ring-cleaving pathways. Preferential hierarchies in substrate utilization and complex transcriptional regulation have been demonstrated to be the norm in many soil bacteria that also contain multiple ring-cleaving pathways. The purpose of this study was to ascertain whether substrate preference exists in S. stellata when the organism is provided a mixture of aromatic compounds that proceed through different ring-cleaving pathways. We focused on the protocatechuate (pca) and the aerobic benzoyl coenzyme A (box) pathways and the substrates known to proceed through them, p-hydroxybenzoate (POB) and benzoate, respectively. When these two substrates were provided at nonlimiting carbon concentrations, temporal patterns of cell density, gene transcript abundance, enzyme activity, and substrate concentrations indicated that S. stellata simultaneously catabolized both substrates. Furthermore, enhanced growth rates were observed when S. stellata was provided both compounds simultaneously compared to the rates of cells grown singly with an equimolar concentration of either substrate alone. This simultaneous-catabolism phenotype was also demonstrated in another lineage member, Ruegeria pomeroyi DSS-3. These findings challenge the paradigm of sequential aromatic catabolism reported for soil bacteria and contribute to the growing body of physiological evidence demonstrating the metabolic versatility of roseobacters.

Hierarchy of Carbon Source Utilization in Soil Bacteria: Hegemonic Preference for Benzoate in Complex Aromatic Compound Mixtures Degraded by Cupriavidus pinatubonensis Strain JMP134

“…If some AC are more available than others, it would make sense that bacteria exposed to those AC evolve more profi- cient metabolic routes (increased uptake, sensitive gene induction, robust and efficient enzymes, better detoxification mechanisms, and fine-tuned metabolic fluxes, among others) for the more abundant than for the less abundant AC, thus improving their competitiveness in such habitats. It should be noted that in seawater, a natural environment not expected to be rich in AC, bacteria would degrade Bz and 4-Hb simultaneously, as reported for Sagittula stellata E-37, a member of the very abundant marine Roseobacter lineage (45). There are contrasting details concerning a putative, relatively high natural abundance of Bz in terrestrial environments.…”

“…Altogether, it seems clear that Bz is a distinctive preferred substrate for several soil bacteria. There are, of course, examples of simultaneous degradation in Bz-containing mixtures (14,44), including synergic interactions such as those described in Sagittula stellata E-37, a member of the Roseobacter lineage, where increased growth rates are found for Bz-4-Hb mixtures (45). There are several possible explanations for the preference for Bz over AC, none of them fully satisfactory.…”

Analysis of Hydroxycinnamic Acid Degradation in Agrobacterium fabrum Reveals a Coenzyme A-Dependent, Beta-Oxidative Deacetylation Pathway

“…Besides A. fabrum, we identified homologs of atu1416, atu1415, atu1417, and atu1421 in S. stellata E-37 (Roseobacter lineage). Remarkably, S. stellata E-37 has been shown able to degrade lignin and to use FA and pCA as primary growth substrates (39,40). Thus, the presence of homologs of Atu1415 (phenylhydroxypropionyl-CoA dehydrogenase) and Atu1421 (HMPKP-CoA ␤-ketothiolase) suggests their putative involvement in lignin degradation by S. stellata E-37 via a coenzyme A-dependent ␤-oxidation deacetylation of FA and/or pCA.…”

Characterization of the interactive effects of labile and recalcitrant organic matter on microbial growth and metabolism

“…LOM, NOM, or mixtures of the two) and the concentrations and sources of the LOM (Table 542 S9). E-37 has been previously shown to simultaneously catabolize aromatic compounds via two 543 different ring cleaving pathways, the benzoyl Co-A and protocatechuate pathways, and derive a 544 beneficial effect when grown on a mixture of carbon substrates compared to either substrate 545 presented alone (Gulvik and Buchan 2013). The metabolic synergy between these two aromatic 546 carbon catabolism pathways may also be a mechanism for OM interactivities that has been 547 previously overlooked.…”