The enigmatic SAR202 cluster up close: shedding light on a globally distributed dark ocean lineage involved in sulfur cycling

Abstract

The dark ocean microbiota represents the unknown majority in the global ocean waters. The SAR202 cluster belonging to the phylum Chloroflexi was the first microbial lineage discovered to specifically inhabit the aphotic realm, where they are abundant and globally distributed. The absence of SAR202 cultured representatives is a significant bottleneck towards understanding their metabolic capacities and role in the marine environment. In this work, we use a combination of metagenome-assembled genomes from deep-sea datasets and publicly available single-cell genomes to construct a genomic perspective of SAR202 phylogeny, metabolism and biogeography. Our results suggest that SAR202 cluster members are medium sized, free-living cells with a heterotrophic lifestyle, broadly divided into two distinct clades. We present the first evidence of vertical stratification of these microbes along the meso- and bathypelagic ocean layers. Remarkably, two distinct species of SAR202 cluster are highly abundant in nearly all deep bathypelagic metagenomic datasets available so far. SAR202 members metabolize multiple organosulfur compounds, many appear to be sulfite-oxidizers and are predicted to play a major role in sulfur turnover in the dark water column. This concomitantly suggests an unsuspected availability of these nutrient sources to allow for the high abundance of these microbes in the deep sea.

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

“…However, the GOS sample from which 90 they were described is actually a freshwater dataset, Lake Gatun (Panama). It is quite evident from 91 our results (Figure 1, Supplementary Figure S2) that this cluster is consistently found only in lakes, 92 up to 30% of the prokaryotic community [24][25][26]. If there are any SAR202 related clades in 103 freshwater habitats they are certainly not very abundant or perhaps did not originate from the water 104 column in the original report [11] (Supplementary Figure S1).…”

“…to class-level taxa. The complete list of datasets used is available in (Mehrshad et al, 2017). Datasets 733 highlighted in gray were used for the assembly.…”

Metabolic Architecture of the Deep Ocean Microbiome

“…The 3hydroxypropionate bi-cycle pathway, which uses HCO3 − as inorganic carbon species, was originally associated with the green nonsulfur bacterium Chloroflexus aurantiacus and with other members of Chloroflexaceae (Strauss andFuchs 1993, Zarzycki et al, 2009). However, individual genes of the pathway have been detected in various strains of Alpha-and Gammaproteobacteria (Zarzycki et al, 2009) and recently in deep ocean SAR202 clade genomes (Landry et al, 2017, Mehrshad et al, 2018. These results not only reflect a ubiquitous role for some inorganic carbon fixation pathways in the deep ocean, highlighting the wide distribution of the Calvin Cycle and the 3-Hydroxypropionate bicycle in both PA and FL microbial communities ( Fig.…”

“…Genes of this pathway have recently been detected within the uncultured SAR202 deep ocean clade genomes related to Chloroflexi, although the role of the 3-Hydroxypropionate bi-cycle in this clade has been linked to the assimilation of intermediate metabolisms produced by the degradation of recalcitrant dissolved organic matter (DOM) rather than for fixing CO2 (Landry et al, 2017). Thus, this clade displays the capacity to metabolize multiple organosulfur compounds and appears to be a sulfite oxidizer (Mehrshad et al, 2018).…”

In situ meta‐omic insights into the community compositions and ecological roles of hadal microbes in the Mariana Trench

“…The aprA genes of the hadal SAR11 clade and Rhodospirillales showed high similarities (>70%) with those of reported SAR11 sulfite‐oxidizers (Thrash et al ., ). Similarly, the aprA genes of the hadal SAR202 clade also resembled homologues from deep‐sea relatives that were considered to be able to oxidize sulfite as well (Mehrshad et al ., ). Together with the finding of taurine dioxygenase and alkanesulfonate monooxygenase, a number of hadal microbial species might utilize the excess sulfite produced by metabolizing organosulfur compounds as an energy source, which suggested their important role playing in sulfur cycle of the extremely deep ocean trench.…”