Tuning fresh: radiation through rewiring of central metabolism in streamlined bacteria

Abstract

Most free-living planktonic cells are streamlined and in spite of their limitations in functional flexibility, their vast populations have radiated into a wide range of aquatic habitats. Here we compared the metabolic potential of subgroups in the Alphaproteobacteria lineage SAR11 adapted to marine and freshwater habitats. Our results suggest that the successful leap from marine to freshwaters in SAR11 was accompanied by a loss of several carbon degradation pathways and a rewiring of the central metabolism. Examples for these are C1 and methylated compounds degradation pathways, the Entner–Doudouroff pathway, the glyoxylate shunt and anapleuretic carbon fixation being absent from the freshwater genomes. Evolutionary reconstructions further suggest that the metabolic modules making up these important freshwater metabolic traits were already present in the gene pool of ancestral marine SAR11 populations. The loss of the glyoxylate shunt had already occurred in the common ancestor of the freshwater subgroup and its closest marine relatives, suggesting that the adaptation to freshwater was a gradual process. Furthermore, our results indicate rapid evolution of TRAP transporters in the freshwater clade involved in the uptake of low molecular weight carboxylic acids. We propose that such gradual tuning of metabolic pathways and transporters toward locally available organic substrates is linked to the formation of subgroups within the SAR11 clade and that this process was critical for the freshwater clade to find and fix an adaptive phenotype.

Metabolic evolution and the self-organization of ecosystems

“…Furthermore, coastal SAR11 strains can replace pyruvate with glucose metabolized via glycolysis, whereas open ocean strains lack glycolysis and have an obligate requirement for pyruvate (97). Similar adaptations are not observed in freshwater strains of SAR11 (98). Thus, oceanic SAR11 populations have evolved a dependency on exactly the compounds (pyruvate and glycolate) that our metabolic reconstructions suggest emerged as excretion pathways in Prochlorococcus ( Fig.…”

“…We mapped the distribution of metabolic genes across clades (SI Appendix, Table S2) onto the phylogeny of marine SAR11 clades to further reconstruct the evolution of their metabolic core (96)(97)(98) (Fig. 5 and SI Appendix, Fig.…”

Competition and niche separation of pelagic bacteria in freshwater habitats

“…). This might in fact be one reason why important taxa of non‐motile bacteria such as the order‐like lineage of acI actinobacteria, harbouring the Candidatus genus Planktophilia (Jezbera et al ., ) or LD12 alphaproteobacteria from the candidate order Pelagibacteriales (also known as the freshwater SAR11‐IIIb lineage) still resist all cultivation attempts (Ghylin et al ., ; Eiler et al ., ), while other predominantly non‐motile genera such as Polynucleobacter spp. require prolonged acclimation to elevated substrate levels before they can be isolated (Hahn et al ., ; Hahn et al ., ).…”

“…Bacterial growth in freshwaters may also be limited by other nutritional requirements, for example, phosphorus (P) (Vadstein, ; Carlsson and Caron, ; Smith and Prairie, ), to the extent that unutilized labile DOC may even accumulate under P limitation (Vadstein et al ., ). Accordingly, freshwater microbes have developed unusual physiological strategies to efficiently grow on trace amounts of P, such as small genomes with medium to low GC content (Hahn et al ., ; Ghylin et al ., ; Salcher et al ., ; Eiler et al ., ), an extremely low RNA content, or modified membrane lipids (Yao et al ., ). Single bacterial strains may be specialized for either pulsed or residual P availability (Vadstein, ), and there are clear differences between major freshwater bacterial lineages in their growth response to P addition (Šimek et al ., ; Salcher et al ., ).…”

“…Flavobacteriaceae that thrive in coastal marine waters during phytoplankton blooms express specific degradation genes for algal polysaccharides in combination with matching transporter systems for oligosaccharides (Teeling et al ., ), pointing at niche separation via substrate specialisation. Moreover, field data of sympatric bacterioplankton populations (Buck et al ., ; Salcher et al ., ) and genomic analyses (Hahn et al ., ; Ghylin et al ., ; Salcher et al ., ; Denef et al ., ; Eiler et al ., ) both suggest that various aquatic bacteria exhibit a conspicuous extent of specialisation for particular LMW DOM compounds, or for DOM derived from particular algae (Šimek et al ., ; Sarmento et al ., ).…”