Phylogenomics of Rhodobacteraceae reveals evolutionary adaptation to marine and non-marine habitats

Abstract

Marine Rhodobacteraceae (Alphaproteobacteria) are key players of biogeochemical cycling, comprise up to 30% of bacterial communities in pelagic environments and are often mutualists of eukaryotes. As ‘Roseobacter clade', these ‘roseobacters' are assumed to be monophyletic, but non-marine Rhodobacteraceae have not yet been included in phylogenomic analyses. Therefore, we analysed 106 genome sequences, particularly emphasizing gene sampling and its effect on phylogenetic stability, and investigated relationships between marine versus non-marine habitat, evolutionary origin and genomic adaptations. Our analyses, providing no unequivocal evidence for the monophyly of roseobacters, indicate several shifts between marine and non-marine habitats that occurred independently and were accompanied by characteristic changes in genomic content of orthologs, enzymes and metabolic pathways. Non-marine Rhodobacteraceae gained high-affinity transporters to cope with much lower sulphate concentrations and lost genes related to the reduced sodium chloride and organohalogen concentrations in their habitats. Marine Rhodobacteraceae gained genes required for fucoidan desulphonation and synthesis of the plant hormone indole 3-acetic acid and the compatible solutes ectoin and carnitin. However, neither plasmid composition, even though typical for the family, nor the degree of oligotrophy shows a systematic difference between marine and non-marine Rhodobacteraceae. We suggest the operational term ‘Roseobacter group' for the marine Rhodobacteraceae strains.

Repeated evolutionary transitions of flavobacteria from marine to non‐marine habitats

“…The interleaved phylogenetic structure of marine and non‐marine groups suggests the transition between marine and non‐marine habitats occurred multiple times along the evolutionary history of Flavobacteriaceae . This is more frequently than what has been observed in both Pelagibacterales and Rhodobacteraceae (Zaremba‐Niedzwiedzka et al ., ; Luo et al ., ; Eiler et al ., , Simon et al ., ). In addition, the interleaved phylogenetic structure of Flavobacteriaceae suggests that the direction of each transition cannot be told through a simple visual examination.…”

“…As a consequence, marine and non‐marine microbes are usually not evolutionarily closely related, and prone to be clustered in distinct lineages (Logares et al ., ). Infrequent ocean‐to‐land transitions have been reported within Alphaproteobacteria lineages including the order Pelagibacterales (Zaremba‐Niedzwiedzka et al ., ; Luo et al ., ; Eiler et al ., ) and the family Rhodobacteraceae (Simon et al ., ), each accompanied with considerable changes in the metabolic repertoire in response to distinct physiochemical conditions and substrate availability.…”

Metabolic versatility of a novel N2‐fixing Alphaproteobacterium isolated from a marine oxygen minimum zone

“…With the aim to provide insights into possible roles of this functional group in the environment, we enriched and isolated a novel diazotroph from waters off the coast of Peru in the ETSP. Genome sequencing revealed the phylogenetic affiliation of the isolate to the family Rhodobacteraceae and, following the operational term suggested by Simon and colleagues (), to the ‘ Roseobacter group’. The distribution and in situ activity of the isolate were determined using fluorescence in situ hybridization (FISH) and stable‐isotope incubation experiments (FISH coupled to secondary ion mass spectrometry).…”

Transcriptional regulation of ectoine catabolism in response to multiple metabolic and environmental cues

“…Building on previous data (Jebbar et al ., ; Schwibbert et al ., ), we have recently proposed a pathway for the complete route of hydroxyectoine/ectoine uptake and catabolism (Schulz et al ., ) (Fig. ) in the marine bacterium Ruegeria pomeroyi DSS‐3 (Moran et al ., ), a member of the widely distributed and metabolically versatile Roseobacter clade (Wagner‐Döbler and Biebl, ; Luo and Moran, ; Simon et al ., ). In this bacterium, import of ectoines is mediated by a high affinity binding‐protein‐dependent and substrate‐inducible TRAP‐type transport system (UehABC) (Lecher et al ., ; Mulligan et al ., ) (Fig.…”