Abstract

In recent years a large number of isolates were obtained from saline environments that are phylogenetically related to distinct clades of oligotrophic marine gammaproteobacteria, which were originally identified in seawater samples using cultivation independent methods and are characterized by high seasonal abundances in coastal environments. To date a sound taxonomic framework for the classification of these ecologically important isolates and related species in accordance with their evolutionary relationships is missing. In this study we demonstrate that a reliable allocation of members of the oligotrophic marine gammaproteobacteria (OMG) group and related species to higher taxonomic ranks is possible by phylogenetic analyses of whole proteomes but also of the RNA polymerase beta subunit, whereas phylogenetic reconstructions based on 16S rRNA genes alone resulted in unstable tree topologies with only insignificant bootstrap support. The identified clades could be correlated with distinct phenotypic traits illustrating an adaptation to common environmental factors in their evolutionary history. Genome wide gene-content analyses revealed the existence of two distinct ecological guilds within the analyzed lineage of marine gammaproteobacteria which can be distinguished by their trophic strategies. Based on our results a novel order within the class Gammaproteobacteria is proposed, which is designated Cellvibrionales ord. nov. and comprises the five novel families Cellvibrionaceae fam. nov., Halieaceae fam. nov., Microbulbiferaceae fam. nov., Porticoccaceae fam. nov., and Spongiibacteraceae fam. nov.

Highlights

  • For several years an increasing effort in the characterization of bacteria from marine environments led to the isolation of a large number of gammaproteobacteria that belong to phylogenetic groups originally defined by 16S rRNA gene sequences retrieved from environmental samples

  • Within the oligotrophic marine gammaproteobacteria (OMG) group members of the OM60/NOR5 and SAR92 clades are of special interest, because cultivation-independent surveys have shown that these bacteria can reach a high seasonal abundance especially in coastal environments (Stingl et al, 2007; Yan et al, 2009)

  • Since the first phylogenetic assessment of the OMG group by Cho and Giovannoni (2004) a large number of isolates with a close phylogenetic relationship to members of the OMG group were cultured and described as novel species. All of these isolates could be either affiliated to the OM60/NOR5 clade or were closely related to members of the BD1-7 and SAR92 clades, whereas no type strains or genome sequenced isolates became available belonging to the OM182 or KI89A clade which prevents a more detailed phylogenetic assessment of the latter two groups

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Summary

Introduction

For several years an increasing effort in the characterization of bacteria from marine environments led to the isolation of a large number of gammaproteobacteria that belong to phylogenetic groups originally defined by 16S rRNA gene sequences retrieved from environmental samples. Within the OMG group members of the OM60/NOR5 and SAR92 clades are of special interest, because cultivation-independent surveys have shown that these bacteria can reach a high seasonal abundance especially in coastal environments (Stingl et al, 2007; Yan et al, 2009). Genome analyses revealed the potential of harvesting light for mixotrophic growth in several members of the OMG group, which made these isolates interesting study objects for further research (e.g., Stingl et al, 2007; Spring and Riedel, 2013). Genes involved in the complex pathway of aerobic anoxygenic photosynthesis were so far only found among members of the OM60/NOR5 clade (Spring et al, 2013, 2014), whereas genes for the synthesis of proteorhodopsin, a light-driven proton pump, seems to be more widely spread and were identified in the genomes of representatives of the SAR92 (Courties et al, 2014), BD1-7 (Oh et al, 2010a), and OM60/NOR5 clades (Jang et al, 2011b)

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