Chloroflexi CL500-11 Populations That Predominate Deep-Lake Hypolimnion Bacterioplankton Rely on Nitrogen-Rich Dissolved Organic Matter Metabolism and C ₁ Compound Oxidation

Abstract

The Chloroflexi CL500-11 clade contributes a large proportion of the bacterial biomass in the oxygenated hypolimnia of deep lakes worldwide, including the world's largest freshwater system, the Laurentian Great Lakes. Traits that allow CL500-11 to thrive and its biogeochemical role in these environments are currently unknown. Here, we found that a CL500-11 population was present mostly in offshore waters along a transect in ultraoligotrophic Lake Michigan (a Laurentian Great Lake). It occurred throughout the water column in spring and only in the hypolimnion during summer stratification, contributing up to 18.1% of all cells. Genome reconstruction from metagenomic data suggested an aerobic, motile, heterotrophic lifestyle, with additional energy being gained through carboxidovory and methylovory. Comparisons to other available streamlined freshwater genomes revealed that the CL500-11 genome contained a disproportionate number of cell wall/capsule biosynthesis genes and the most diverse spectrum of genes involved in the uptake of dissolved organic matter (DOM) substrates, particularly peptides. In situ expression patterns indicated the importance of DOM uptake and protein/peptide turnover, as well as type I and type II carbon monoxide dehydrogenase and flagellar motility. Its location in the water column influenced its gene expression patterns the most. We observed increased bacteriorhodopsin gene expression and a response to oxidative stress in surface waters compared to its response in deep waters. While CL500-11 carries multiple adaptations to an oligotrophic lifestyle, its investment in motility, its large cell size, and its distribution in both oligotrophic and mesotrophic lakes indicate its ability to thrive under conditions where resources are more plentiful. Our data indicate that CL500-11 plays an important role in nitrogen-rich DOM mineralization in the extensive deep-lake hypolimnion habitat. Freshwater lakes are disproportionally active sites of carbon cycling relative to the surface area that they cover due to strong linkages to the surrounding land, from which they receive inorganic nutrients as well as organic carbon (1, 2). Of the estimated 1.9 Pg of terrestrial organic carbon that freshwater systems process per year, nearly half is respired by bacteria (3-5). When soil dissolved organic carbon outgassing is included, net freshwater carbon emissions are of the same order of magnitude as net oceanic uptake (2). While photochemical mineralization of organic carbon can predominate in lake habitats with high levels of photosynthetically active radiation (6), bacterial contributions to dissolved organic matter (DOM) mineralization are important as well (7).Nevertheless, linkages between the metabolism of organic carbon and specific populations remain limited, particularly in the less-studied hypolimnia of lakes, even for ubiquitous and highly abundant taxa, due to challenges with the isolation of representatives of these taxa (8). In recent years, the use of culture-independent methods has provided ins...

Spatiotemporal distribution of bacterioplankton functional groups along a freshwater estuary to pelagic gradient in Lake Michigan

“…1, Table 1). The sites in Lake Michigan are the same sites used by Denef et al (2016) to characterize Chloroflexi abundance and function. During the summer sampling, water samples were also collected from a deep-chlorophyll maximum (DCM) layer (35 m) at the M110 station.…”

Hidden in plain sight - highly abundant and diverse planktonic freshwater Chloroflexi

“…Originally described from Crater 55 Lake (USA) (>300m depth) using 16S rRNA clone library and oligonucleotide probe hybridization 56 [11, 12], these microbes have been found to constitute consistently large fractions of prokaryotic 57 communities (up to 26%) in deep lake hypolimnia all over the world [11][12][13][14][15][16]. The only genomic 58 insights into their lifestyle come from a single metagenomic assembled genome (MAG) from Lake 59Michigan (estimated completeness 90%) along with in situ expression patterns that revealed 60 CL500-11 to be flagellated, aerobic, photoheterotrophic bacteria, playing a major role in 61 demineralization of nitrogen-rich dissolved organic matter in the hypolimnion [16]. Another lineage 62 is the CL500-9 cluster [11], that was described as a freshwater sister lineage of the marine SAR202 63 cluster (now class 'Ca.…”

Lake Bacterial Assemblage Composition Is Sensitive to Biological Disturbance Caused by an Invasive Filter Feeder

“…Despite these limitations, we are confident about the main shift that was inferred, which was a strong increase in the predominance of heterotrophic chemoorganotrophs predicted to be capable of energy generation using rhodopsin. Genomic analyses of the affected taxonomic groups inferred to have these metabolic traits (predominantly acI Actinobacteria , but also LD12 and CL500-11) are consistently retrieving the genes encoding these traits (42, 49, 50). …”