Complete ecological isolation and cryptic diversity in Polynucleobacter bacteria not resolved by 16S rRNA gene sequences

Abstract

Transplantation experiments and genome comparisons were used to determine if lineages of planktonic Polynucleobacter almost indistinguishable by their 16S ribosomal RNA (rRNA) sequences differ distinctively in their ecophysiological and genomic traits. The results of three transplantation experiments differing in complexity of biotic interactions revealed complete ecological isolation between some of the lineages. This pattern fits well to the previously detected environmental distribution of lineages along chemical gradients, as well as to differences in gene content putatively providing adaptation to chemically distinct habitats. Patterns of distribution of iron transporter genes across 209 Polynucleobacter strains obtained from freshwater systems and representing a broad pH spectrum further emphasize differences in habitat-specific adaptations. Genome comparisons of six strains sharing ⩾99% 16S rRNA similarities suggested that each strain represents a distinct species. Comparison of sequence diversity among genomes with sequence diversity among 240 cultivated Polynucleobacter strains indicated a large cryptic species complex not resolvable by 16S rRNA sequences. The revealed ecological isolation and cryptic diversity in Polynucleobacter bacteria is crucial in the interpretation of diversity studies on freshwater bacterioplankton based on ribosomal sequences.

Spatiotemporal analysis of microbial community dynamics during seasonal stratification events in a freshwater lake (Grand Lake, OK, USA)

“…Members of the Beta-Proteobacteria decreased in abundances from June to September in both PA and FL fractions, but were significantly higher in the FL fraction in September (Fig 6A) (Student t-test P-value = 0.0001). Members of Polynucleobacter , a ubiquitous and abundant lineage in freshwater habitats with representatives that exist both as free-living organisms as well as endosymbionts of freshwater ciliates [97], were significantly more abundant in the FL fraction in September (Student t-test P-value = 0.019), consistent with previous reports of its abundance in freshwater planktonic fraction [98]. On the other hand, members of the Azohydromonas , a heterotrophic polyhydroxybutrate-synthesizing bacterium commonly isolated from soil [99], as well as unclassified members of the family Comamonadaceae, common members of freshwater lakes communities [84], were more abundant in the PA fraction in September (Fig 6E).…”

Spatiotemporal distribution and microbial assimilation of polyamines in a mesotrophic lake

“…Genome sequences of Limnohabitans planktonicus (Kasalický et al ) and other Limnohabitans isolates (Zeng et al, ) also indicate the presence of polyamine transporters. In contrast, no such uptake mechanism was found in members of the Polynucleobacter ‐C cluster (Hahn et al ) which agrees with our MAR analyses. This points at differences in substrate preferences between these sympatric betaproteobacterial lineages, as has been shown before for other labile DOC compounds (Salcher et al ).…”

Higher contribution of globally rare bacterial taxa reflects environmental transitions across the surface ocean

“…It is notable that two OTUs were still categorized as normal‐like even when all depths and size fractions were included (Figure d), suggesting a remarkable versatility of a few taxa within communities (Supporting Information Table ). Alternatively, the cosmopolitanism shown by some community members might be the result of hidden diversity that cannot be resolved with the 16S rRNA marker, since identical 16S rRNA sequences can represent different ecotypes (e.g., Hahn, Jezberová, Koll, Saueressig‐Beck, & Schmidt, ; Farrant et al, ). Indeed, 22 out of our 68 surface normal‐like OTUs matched more than one publicly available genome at ≥99% similarity level (Supporting Information Figure ), although it remains unknown whether these cosmopolitan OTUs represented one or several genomes.…”