Rolf Daniel
Meinhard Simon2
Bernd Wemheuer- 1Genomic and Applied Microbiology and Göttingen Genomics Laboratory, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany
- 2Biology of Geological Processes, Institute for Chemistry and Biology of the Marine Environment, University of Oldenburg, Oldenburg, Germany
- 3Centre for Marine Bio-Innovation, The University of New South Wales, Sydney, NSW, Australia
- 4School of Biological Earth and Environmental Sciences, The University of New South Wales, Sydney, NSW, Australia
Editorial on the Research Topic
Molecular Ecology and Genetic Diversity of the Roseobacter Clade
The Roseobacter clade, more recently referred to as Roseobacter group, is a paraphyletic group within the Rhodobacteraceae (Alphaproteobacteria) (Simon et al., 2017). It is one of the most widely distributed and abundant bacterial groups in the marine ecosystem constituting up to 30% of bacterial communities in pelagic environments. Roseobacter group members inhabit a great variety of marine habitats and niches. They exhibit a free-living or surface-associated lifestyle and even occur in oxic and anoxic sediments (Luo and Moran, 2014). They are physiologically and genetically very versatile. Some of the important functional traits found in the Roseobacter group are the utilization of various organic and inorganic compounds including the catabolism of dimethylsulfoniopropionate (DMSP), energy acquisition by sulfur oxidation, aerobic anoxygenic photosynthesis and carbon monoxide oxidation, and the production of secondary metabolites (Buchan et al., 2005; Wagner-Döbler and Biebl, 2006; Brinkhoff et al., 2008; Todd et al., 2012).
Although various aspects of the Roseobacter group have been studied in recent years (e.g., Luo and Moran, 2014; Wemheuer et al., 2014, 2017; Gram et al., 2015; Voget et al., 2015; Lutz et al., 2016; Zhang et al., 2016), our knowledge about its ecological significance and the evolutionary processes shaping the genomes of this group is still limited. The 10 publications presented in this research topic “Molecular Ecology and Genetic Diversity of the Roseobacter Clade” highlight new and interesting findings on the evolution, biodiversity, and functions of the Roseobacter group in the marine environment. Contributions include original research, a perspective, and a comprehensive review.
In three contributions, culture-independent approaches are employed to assess the abundance and distribution of Roseobacter group members in marine pelagic systems (Bakenhus et al.; Freese et al.) and Pacific sediments (Pohlner et al.). Bakenhus et al. highlight the major role of several pelagic members of the Roseobacter group in processing phytoplankton-derived organic matter, although this group constituted only a minor proportion of the total bacterioplankton community. Freese et al. show that a previously unknown, distinct group of Phaeobacter gallaeciensis possess a limited number of group-specific genes, which may be relevant for its association with mesozooplankton and for its colonization in marine pelagic systems.
As most studies on the abundance and diversity of the Roseobacter group were conducted on pelagic samples (e.g., Giebel et al., 2011; Wemheuer et al., 2015; Billerbeck et al., 2016), the distribution and function of this group in sediments is less understood (but see Kanukollu et al., 2015). In their contribution, Pohlner et al. demonstrate that different oligo- and ultraoligotrophic oceanic provinces in the subtropics and tropics of the Pacific were characterized by specific sediment communities and Roseobacter group members, distinct from those of the more productive temperate and subarctic regions. Roseobacter-affiliated OTUs were dominated by uncultured members, demonstrating the need to obtain cultured Roseobacter representatives from sediments to link community structures to specific metabolic processes at the seafloor.
Aside from community patterns, the functional response of the ambient bacterial community toward a Phaeocystis globosa bloom in the southern North Sea was studied using metaproteomic approaches (Wöhlbrand et al.) This study highlights the application of different sample preparation techniques and mass spectrometric methods for a comprehensive characterization of marine bacterioplankton responses to changing environmental conditions. The comprehensive approach verified previous metaproteomic studies of marine bacterioplankton (e.g., Sowell et al., 2011; Teeling et al., 2012; Georges et al., 2014), but also revealed new insights into carbon and nitrogen metabolism.
Gardiner et al. demonstrate for the first time temperature-dependent regulation of the RTX-like proteins in the important seaweed pathogen Nautella italica R11 and thus provides the basis for future functional studies on the temperature-dependent manner of secreted proteins and their role in pathogenicity and/or environmental persistence of N. italica R11. This is of crucial importance as increasing ocean temperatures associated with climate change are predicted to cause greater host stress and more extensive disease events in macroalgae.
Two studies focused on adaptations to environmental properties of the Roseobacter group (Bullock et al.; Ebert et al.) Ebert et al. describe for the first time a regulatory network solely composed of four Crp/Fnr-family regulators responsible for the metabolic adaptation to low oxygen tension observed in the marine bacterium Dinoroseobacter shibae. Bullock et al. review the evolution of DMSP metabolism in marine phytoplankton and bacteria, thereby illustrating that the enzymes of DMSP demethylation and cleavage pathways are examples of the various processes of enzyme adaptation and evolution, which occurred within the Roseobacter group in the last 250 million years.
N-acyl-homoserine lactones (AHLs) constitute the major class of semiochemicals in quorum sensing (QS) systems (Williams, 2007; Papenfort and Bassler, 2016). Complex mixtures of AHLs have been found for the several members of the Roseobacter clade (Wagner-Döbler et al., 2005). In their contribution, Doberva et al. discover an unsuspected capacity of the marine Rhodobacteraceae strain MOLA 401 to synthesize 20 different putative AHLs by a combination of biosensor-based screening and liquid chromatography coupled to mass spectrometry and nuclear magnetic resonance. The authors conclude that the higher diversity of signaling molecules, unusual for a single strain, shows new molecular adaptations of QS systems to planktonic life.
Horizontal gene transfer (HGT) is an important driver of bacterial diversification and the evolution of prokaryotic genomes (Polz et al., 2013; Sun et al., 2015). Two articles in this research topic highlight the importance of HGT in the Roseobacter group. Bartling et al. identified a Roseobacter-specific RepABC-type operon in the draft genome of the marine rhizobium Martelella mediterranea DSM 17316T, whereas Petersen and Wagner -Döbler provide the first evidence for conjugational plasmid transfer across biogeographical and phylogenetic barriers in the Rhodobacteraceae.
In summary, the articles presented in this research topic demonstrate the benefits of using multidisciplinary approaches to analyze and deepen our knowledge of the ecological significance, functions, and the evolutionary processes shaping the genomic basis and responses of the Roseobacter group to environmental conditions. Moreover, many challenges and questions were identified that remain to be addressed. We thank all the participating authors for their contributions, which we believe will be the basis for future investigations into the function, evolution, and diversity of the fascinating Roseobacter group.
Author Contributions
All authors listed have made a substantial, direct, and intellectual contribution to the work, and approved it for publication.
Funding
This work was supported by the Deutsche Forschungsgemeinschaft (DFG) within the Collaborative Research Center Roseobacter (TRR51).
Conflict of Interest Statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
References
Billerbeck, S., Wemheuer, B., Voget, S., Poehlein, A., Giebel, H.-A., Brinkhoff, T., et al. (2016). Biogeography and environmental genomics of the Roseobacter group affiliated pelagic CHAB-I-5 lineage. Nat. Microbiol. 1:16063. doi: 10.1038/nmicrobiol.2016.63
Brinkhoff, T., Giebel, H. A., and Simon, M. (2008). Diversity, ecology, and genomics of the Roseobacter clade: a short overview. Arch. Microbiol. 189, 531–539. doi: 10.1007/s00203-008-0353-y
Buchan, A., González, J. M., and Moran, M. A. (2005). Overview of the marine roseobacter lineage. Appl. Environ. Microbiol. 71, 5665–5677. doi: 10.1128/AEM.71.10.5665-5677.2005
Georges, A. A., El-Swais, H., Craig, S. E., Li, W. K. W., and Walsh, D. A. (2014). Metaproteomic analysis of a winter to spring succession in coastal northwest Atlantic Ocean microbial plankton. ISME J. 8, 1301–1313. doi: 10.1038/ismej.2013.234
Giebel, H. A., Kalhoefer, D., Lemke, A., Thole, S., Gahl-Janssen, R., Simon, M., et al. (2011). Distribution of Roseobacter RCA and SAR11 lineages in the North Sea and characteristics of an abundant RCA isolate. ISME J. 5, 8–19. doi: 10.1038/ismej.2010.87
Gram, L., Rasmussen, B. B., Wemheuer, B., Bernbom, N., Ng, Y. Y., Porsby, C. H., et al. (2015). Phaeobacter inhibens from the Roseobacter clade has an environmental niche as a surface colonizer in harbors. Syst. Appl. Microbiol. 38, 483–493. doi: 10.1016/j.syapm.2015.07.006
Kanukollu, S., Wemheuer, B., Herber, J., Billerbeck, S., Lucas, J., Daniel, R., et al. (2015). Distinct compositions of free-living, particle-associated and benthic communities of the Roseobacter group in the North Sea. FEMS Microbiol. Ecol. 92:145. doi: 10.1093/femsec/fiv145
Luo, H., and Moran, M. A. (2014). Evolutionary ecology of the marine Roseobacter clade. Microbiol. Mol. Biol. Rev. 78, 573–587. doi: 10.1128/MMBR.00020-14
Lutz, C., Thomas, T., Steinberg, P., Kjelleberg, S., and Egan, S. (2016). Effect of interspecific competition on trait variation in Phaeobacter inhibens biofilms. Environ. Microbiol. 18, 1635–1645. doi: 10.1111/1462-2920.13253.
Papenfort, K., and Bassler, B. L. (2016). Quorum sensing signal–response systems in Gram-negative bacteria. Nat. Rev. Microbiol. 14, 576–588. doi: 10.1038/nrmicro.2016.89
Polz, M. F., Alm, E. J., and Hanage, W. P. (2013). Horizontal gene transfer and the evolution of bacterial and archaeal population structure. Trends Genet. 29, 170–175. doi: 10.1016/j.tig.2012.12.006
Simon, M., Scheuner, C., Meier-Kolthoff, J. P., Brinkhoff, T., Wagner-Döbler, I., Ulbrich, M., et al. (2017). Phylogenomics of Rhodobacteraceae reveals evolutionary adaptation to marine and non-marine habitats. IMSE J. 11, 1483–1499. doi: 10.1038/ismej.2016.198
Sowell, S. M., Abraham, P. E., Shah, M., Verberkmoes, N. C., Smith, D. P., Barofsky, D. F., et al. (2011). Environmental proteomics of microbial plankton in a highly productive coastal upwelling system. ISME J. 5, 856–865. doi: 10.1038/ismej.2010.168
Sun, B.-F., Li, T., Xiao, J.-H., Jia, L.-Y., Liu, L., Zhang, P., et al. (2015). Horizontal functional gene transfer from bacteria to fishes. Sci. Rep. 5:18676. doi: 10.1038/srep18676
Teeling, H., Fuchs, B. M., Becher, D., Klockow, C., Gardebrecht, A., Bennke, C. M., et al. (2012). Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336, 608–611. doi: 10.1126/science.1218344.
Todd, J. D., Kirkwood, M., Newton-Payne, S., and Johnston, A. W. B. (2012). DddW, a third DMSP lyase in a model Roseobacter marine bacterium, Ruegeria pomeroyi DSS-3. ISME J. 6, 223–226. doi: 10.1038/ismej.2011.79.
Voget, S., Wemheuer, B., Brinkhoff, T., Vollmers, J., Dietrich, S., Giebel, H.-A., et al. (2015). Adaptation of an abundant Roseobacter RCA organism to pelagic systems revealed by genomic and transcriptomic analyses. ISME J. 9, 371–384. doi: 10.1038/ismej.2014.134
Wagner-Döbler, I., and Biebl, H. (2006). Environmental biology of the marine Roseobacter lineage. Annu. Rev. Microbiol. 60, 255–280. doi: 10.1146/annurev.micro.60.080805.142115
Wagner-Döbler, I., Thiel, V., Eberl, L., Allgaier, M., Bodor, A., Meyer, S., Ebner, S., et al. (2005). Discovery of complex mixtures of novel long-chain quorum sensing signals in free-living and host-associated marine alphaproteobacteria. Chembiochem 6, 2195–2206. doi: 10.1002/cbic.200500189
Wemheuer, B., Güllert, S., Billerbeck, S., Giebel, H.-A., Voget, S., Simon, M., et al. (2014). Impact of a phytoplankton bloom on the diversity of the active bacterial community in the southern North Sea as revealed by metatranscriptomic approaches. FEMS Microbiol. Ecol. 87, 378–389. doi: 10.1111/1574-6941.12230
Wemheuer, B., Wemheuer, F., Hollensteiner, J., Meyer, F.-D., Voget, S., and Daniel, R. (2015). The green impact: bacterioplankton response towards a phytoplankton spring bloom in the southern North Sea assessed by comparative metagenomic and metatranscriptomic approaches. Front. Microbiol. 6:805. doi: 10.3389/fmicb.2015.00805
Wemheuer, B., Wemheuer, F., Meier, D., Billerbeck, S., Giebel, H.-A., Simon, M., et al. (2017). Linking compositional and functional predictions to decipher the biogeochemical significance in DFAA turnover of abundant bacterioplankton lineages in the North Sea. Microorganisms 5:E68. doi: 10.3390/microorganisms5040068
Williams, P. (2007). Quorum sensing, communication and cross-kingdom signalling in the bacterial world. Microbiology 153, 3923–3938. doi: 10.1099/mic.0.2007/012856-0
Keywords: Roseobacter group, microbial ecology, microbial evolution, molecular ecology, microbial diversity
Citation: Daniel R, Simon M and Wemheuer B (2018) Editorial: Molecular Ecology and Genetic Diversity of the Roseobacter Clade. Front. Microbiol. 9:1185. doi: 10.3389/fmicb.2018.01185
Received: 21 March 2018; Accepted: 16 May 2018;
Published: 01 June 2018.
Edited by:
Alison Buchan, University of Tennessee, Knoxville, United StatesReviewed by:
Jose M. Gonzalez, Universidad de La Laguna, SpainCopyright © 2018 Daniel, Simon and Wemheuer. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Bernd Wemheuer, bwemheu@gwdg.de