Ecophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes

Abstract

Freshwater Verrucomicrobia spp. are cosmopolitan in lakes and rivers, and yet their roles and ecophysiology are not well understood, as cultured freshwater Verrucomicrobia spp. are restricted to one subdivision of this phylum. Here, we greatly expanded the known genomic diversity of this freshwater lineage by recovering 19 Verrucomicrobia draft genomes from 184 metagenomes collected from a eutrophic lake and a humic bog across multiple years. Most of these genomes represent the first freshwater representatives of several Verrucomicrobia subdivisions. Genomic analysis revealed Verrucomicrobia to be potential (poly)saccharide degraders and suggested their adaptation to carbon sources of different origins in the two contrasting ecosystems. We identified putative extracellular electron transfer genes and so-called “Planctomycete-specific” cytochrome c-encoding genes and identified their distinct distribution patterns between the lakes/layers. Overall, our analysis greatly advances the understanding of the function, ecophysiology, and distribution of freshwater Verrucomicrobia, while highlighting their potential role in freshwater carbon cycling.

Microbial life under ice: Metagenome diversity and in situ activity of Verrucomicrobia in seasonally ice‐covered Lakes

“…In this study, we conducted the first meta‐omics assessment of bacterial metabolism and gene expression patterns in seasonally ice‐covered lakes. In combination with other recent metagenomic studies (Cabello‐Yeves et al ., , b; He et al ., ), our findings contribute to the emerging view that Verrucomicrobia is an important, but previously overlooked component of lake microbial ecosystems. The association of Verrucomicrobia MAGs with ice‐covered conditions suggests certain populations exhibit a winter preference.…”

“…A was inferred from a concatenated alignment of four of the five proteins used in He et al . (), but exhibited a similar topology to a phylogeny generated based on hundreds of proteins (Supporting Information Fig. S2).…”

“…The MAGs were distributed across the CCA plot, and are therefore representative of the observed phylogenetic diversity, biogeography, and seasonal associations of Verrucomicrobia MAGs. A concatenated protein phylogeny that included 43 additional MAGs from Wisconsin lakes (He et al ., ), Lake Baikal (Cabello‐Yeves et al ., ) and the Tous and Amadorio reservoirs in Spain (Cabello‐Yeves et al ., ) was generated in order to place the Quebec MAGs in the context of known Verrucomicrobia genomic diversity (Fig. A).…”

“…A concatenated gene phylogeny tree was created based on 4 of the 5 genes as in He et al . (), in which the 15 Quebec MAGs were put in the contact of the 19 MAGs from Lake Mendota and Trout Bog (Wisconsin), and 7 MAGs from ice‐covered Lake Baikal (Cabello‐Yeves et al ., ) and 17 MAGs from the Tous and Amadorio reservoirs (Cabello‐Yeves et al ., ). Because none of the 15 MAGs in our study contained the DNA polymerase III beta subunit (but had other subunits such as alpha), the concatenated gene phylogeny contained instead the following four genes: TIGR01391 (DNA primase), TIGR01011 (Small subunit ribosomal protein S2), TIGR00460 (Methionyl‐tRNA‐formyltransferase) and TIGR00362 (Chromosomal replication initiation factor).…”

“…For example, analyses of single cell‐amplified genomes (SAGs) and metagenome‐assembled genomes (MAGs) from coastal environments identified preferences for laminarin, xylan (Martinez‐Garcia et al ., ), cellulose and chitin polymers (Herlemann et al ., ). Recently, comparative analysis of Verrucomicrobia MAGs from eutrophic Lake Mendota and dystrophic Trout Bog in Wisconsin, The United States showed differences in the number and type of glycoside hydrolases (GHs) between the two systems, reflecting adaptations to local environments and carbon substrate availability (He et al ., ). Additionally, MAGs from freshwater reservoirs in Spain also suggested a preference for polysaccharides, but also identified genes for the light driven proton pump rhodopsin as well as genes for nitrogen fixation (Cabello‐Yeves et al ., ).…”