Genomic potential for arsenic efflux and methylation varies among global Prochlorococcus populations

Abstract

The globally significant picocyanobacterium Prochlorococcus is the main primary producer in oligotrophic subtropical gyres. When phosphate concentrations are very low in the marine environment, the mol:mol availability of phosphate relative to the chemically similar arsenate molecule is reduced, potentially resulting in increased cellular arsenic exposure. To mediate accidental arsenate uptake, some Prochlorococcus isolates contain genes encoding a full or partial efflux detoxification pathway, consisting of an arsenate reductase (arsC), an arsenite-specific efflux pump (acr3) and an arsenic-related repressive regulator (arsR). This efflux pathway was the only previously known arsenic detox pathway in Prochlorococcus. We have identified an additional putative arsenic mediation strategy in Prochlorococcus driven by the enzyme arsenite S-adenosylmethionine methyltransferase (ArsM) which can convert inorganic arsenic into more innocuous organic forms and appears to be a more widespread mode of detoxification. We used a phylogenetically informed approach to identify Prochlorococcus linked arsenic genes from both pathways in the Global Ocean Sampling survey. The putative arsenic methylation pathway is nearly ubiquitously present in global Prochlorococcus populations. In contrast, the complete efflux pathway is only maintained in populations which experience extremely low PO4:AsO4, such as regions in the tropical and subtropical Atlantic. Thus, environmental exposure to arsenic appears to select for maintenance of the efflux detoxification pathway in Prochlorococcus. The differential distribution of these two pathways has implications for global arsenic cycling, as their associated end products, arsenite or organoarsenicals, have differing biochemical activities and residence times.

Complete arsenic-based respiratory cycle in the marine microbial communities of pelagic oxygen-deficient zones

“…The analysis of WGS assemblies shows the presence of aioA and aioA-like in genomes and thus the potential for microbial arsenite oxidation is not restricted only to oxygen deficient waters. The presence of these sequences in oxygenated waters may be the signature of aerobic chemoautotrophic arsenite oxidation (36), or may be associated with arsenic detoxification processes in regions of phosphate stress (8,37).…”

“…Reads were combined into a single blast database using blast 2.2.28 (47,48) and queried with tblastn (evalue cutoff 1 × 10 −5 ) using full-length known reference sequences, including full-length identified environmental arsenotrophy sequences assembled in this work. Translation of blast recruited reads which were at least 33 amino acids in length after quality trimming were then identified using a phylogenetically informed placement approach by comparison with known reference sequences (20,37,(57)(58)(59). To obtain the abundance of these reads relative to the overall prokaryotic community in the two size fractions, the length-normalized number of identified read pairs for each gene was compared with the lengthnormalized abundance of the single-copy core gene RNA polymerase (rpoB) in the sequenced prokaryotic community (20,37).…”

“…A similar read recruitment and phylogenetic placement method was used to identify reads from ODZ metatranscriptomes (37,(57)(58)(59). Publicly available metatranscriptomes from oxygen deficient zones in the ETNP (39), ETSP (41), and within a sulfide plume in the ETSP (40) were downloaded locally.…”

The rise of oxygen-driven arsenic cycling at ca. 2.48 Ga

“…This is followed by intracellular As(V) reduction via cytoplasmic As(V)-reductases and the extrusion of As(III) by membrane transporters (Fig. 3C) (Dyhrman and Haley, 2011;Wurl et al, 2013Wurl et al, , 2015Yan et al, 2014;Sánchez-Riego et al, 2014;Saunders and Rocap, 2016). The conversion of As(V) to As(III) minimizes phosphate loss, as physicochemical similarities between As(V) and phosphate complicates differentiation by the cell.…”

Unlocking the genomic taxonomy of theProchlorococcuscollective

“…Ecological transitions and changes in the oceans trigger natural genetic engineering and genome changes on a massive scale [25,143]. The PC has evolved in multiple ecologic niches in the global ocean and participates in relevant biogeochemical cycles, such as the recently postulated parasitic arsenic cycle between Eurycolium and Pelagibacter ubique [144,145]. We demonstrated here that the current PC is a diverse group of genera that are clearly distinguishable by eco-genomics.…”