Cultivable Winogradskyella species are genomically distinct from the sympatric abundant candidate species

Carlota Alejandre-Colomo,Bernhard M Fuchs,Rudolf Amann,Tomeu Viver,Jens Harder,Ben Francis,Ramon Rossello-Mora

doi:10.1038/s43705-021-00052-w

Abstract

Winogradskyella is a genus within the phylum Bacteroidetes with a clear marine origin. Most members of this genus have been found associated with marine animals and algae, but also with inorganic surfaces such as sand. In this study, we analyzed genomes of eleven species recently isolated from surface seawater samples from the North Sea during a single spring algae bloom. Corresponding metagenomes yielded a single Candidatus species for this genus. All species in culture, with the exception of W. ursingii, affiliated with a Winogradskyella lineage characterized by large genomes (~4.3 ± 0.4 Mb), with high complexity in their carbohydrate and protein degradation genes. Specifically, the polysaccharide utilization loci (PULs) were diverse within each individual strain, indicating large substrate versatility. Although present in the North Sea, the abundances of these strains were at, or below, the detection limit of the metagenomes. In contrast, the single species, classified as Candidatus W. atlantica, to which all North Sea MAGs belonged, affiliated with a lineage in which the cultivated representatives showed small genomes of ~3.0–3.5 Mb, with the MAGs having ~2.3 Mb. In Ca. W. atlantica, genome streamlining has apparently resulted in the loss of biosynthesis pathways for several amino acids including arginine, methionine, leucine and valine, and the PUL loci were reduced to a single one for utilizing laminarin. This as-yet uncultivated species seems to capitalize on sporadically abundant substrates that are released by algae blooms, mainly laminarin. We also suggest that this streamlined genome might be responsible for the lack of growth on plates for this Candidatus species, in contrast to growth of the less abundant but coexisting members of the genus.

Highlights

Marine microbiologists commonly find that environmentally abundant taxa are challenging to cultivate (e.g. [1,2,3,4,5,6]), while many rare taxa can be cultivated quite readily on plates and in liquid media
We described eight novel species of the Bacteroidetes genus Winogradskyella, a widespread marine genus typically isolated from macroalgae [8,9,10] and marine invertebrates [11,12,13]
We described the novel candidate species Candidatus W. atlantica, based on 14 metagenome-assembled genomes (MAGs) recovered from sampling campaigns across multiple spring blooms [14]

Summary

Introduction

Marine microbiologists commonly find that environmentally abundant taxa are challenging to cultivate (e.g. [1,2,3,4,5,6]), while many rare taxa can be cultivated quite readily on plates and in liquid media. The discrepancy in cultivation success has resulted in disjunct sets of genomic and physiological data for cultivated versus environmental taxa (see, for example, the elucidation of nitrogen fixation in cultivated and uncultivated cyanobacteria [7] and the identification of diazotrophy genes in other phyla [3]). There is an incentive to better understand how to cultivate ecologically relevant taxa in order to be able to test hypotheses generated from the analysis of genomic and metagenomic data. We described eight novel species of the Bacteroidetes genus Winogradskyella, a widespread marine genus typically isolated from macroalgae [8,9,10] and marine invertebrates [11,12,13]. We described the novel candidate species Candidatus W. atlantica, based on 14 metagenome-assembled genomes (MAGs) recovered from sampling campaigns across multiple spring blooms [14]

Methods

Results

Conclusion