The AEGEAN-169 clade of bacterioplankton is synonymous with SAR11 subclade V (HIMB59) and metabolically distinct

Abstract

Bacterioplankton of the SAR11 clade are the most abundant marine microorganisms and consist of numerous subclades spanning order-level divergence ( Pelagibacterales ). The assignment of the earliest diverging subclade V (a.k.a. HIMB59) to the Pelagibacterales is highly controversial, with multiple recent phylogenetic studies placing them completely separate from SAR11. Other than through phylogenomics, subclade V has not received detailed examination due to limited genomes from this group. Here, we assessed the ecogenomic characteristics of subclade V to better understand the role of this group in comparison to the Pelagibacterales . We used a new isolate genome, recently released single-amplified genomes and metagenome-assembled genomes, and previously established SAR11 genomes to perform a comprehensive comparative genomics analysis. We paired this analysis with the recruitment of metagenomes spanning the open ocean, coastal, and brackish systems. Phylogenomics, average amino acid identity, and 16S rRNA gene phylogeny indicate that SAR11 subclade V is synonymous with the ubiquitous AEGEAN-169 clade and support the contention that this group represents a taxonomic family. AEGEAN-169 shared many bulk genome qualities with SAR11, such as streamlining and low GC content, but genomes were generally larger. AEGEAN-169 had overlapping distributions with SAR11 but was metabolically distinct from SAR11 in its potential to transport and utilize a broader range of sugars as well as in the transport of trace metals and thiamin. Thus, regardless of the ultimate phylogenetic placement of AEGEAN-169, these organisms have distinct metabolic capacities that likely allow them to differentiate their niche from canonical SAR11 taxa. IMPORTANCE One goal of marine microbiologists is to uncover the roles various microorganisms are playing in biogeochemical cycles. Success in this endeavor relies on differentiating groups of microbes and circumscribing their relationships. An early-diverging group (subclade V) of the most abundant bacterioplankton, SAR11, has recently been proposed as a separate lineage that does not share a most recent common ancestor. But beyond phylogenetics, little has been done to evaluate how these organisms compare with SAR11. Our work leverages dozens of new genomes to demonstrate the similarities and differences between subclade V and SAR11. In our analysis, we also establish that subclade V is synonymous with a group of bacteria established from 16S rRNA gene sequences, AEGEAN-169. Subclade V/AEGEAN-169 has clear metabolic distinctions from SAR11 and their shared traits point to remarkable convergent evolution if they do not share a most recent common ancestor.

Phosphate-related genomic islands as drivers of environmental adaptation in the streamlined marine alphaproteobacterial HIMB59

“…Although GCA002718135-1.A was present in a larger number of stations, the highest mean recruitment value was found in the HIMB59-1.A genomospecies (median RPKG [number of recruited reads per kb of genome per Gb of metagenome] 32.6) (Table S3). The classification of genomospecies as well as their distribution corroborates and extends the recent work of Getz et al ( 14 ). The correlation in nomenclature between the groups described in both studies can be found in Table S1.…”

“…In order to complement the genomospecies information, we analyzed the genetic determinants that differentiated the three main genomospecies. This information, detailed in the supplementary material, not only extends the data previously obtained ( 14 ) but also puts the results in perspective by comparing them with several groups of marine microbes with which they share habitat. These results revealed an important role of galactose metabolism in all members of this order.…”

“…The HIMB59 clade, with only two representatives obtained in pure culture ( 10 , 11 ), was originally described as clade V within the order Pelagibacterales (SAR11 clade) ( 10 ). However, several phylogenomic studies ( 12 – 14 ), as well as genomic classification based on the Genome Taxonomy Database (GTDB) ( 15 ), have classified these genomes as a different order to the Pelagibacterales . Before obtaining the first pure culture, the first sequences obtained from DNA-based clone libraries (16S rRNA genes) designated the group as AEGEAN-169 marine group ( 16 ).…”

Microbial ecology of coastal northern Gulf of Mexico waters

“…Many of these groups are typically considered “marine” or “freshwater” taxa. Nevertheless, in addition to the nGoM, these taxa have been observed in brackish environments such as the Baltic Sea, Chilika Lagoon (Bay of Bengal), and the Chesapeake and San Francisco Bays (Campbell and Kirchman 2012; D’Ambrosio et al 2014; Hugerth et al 2015; Mohapatra et al 2020; Rasmussen et al 2020; Wang et al 2020; Getz et al 2023). Thus, our study expands the known biogeography and salinity ranges of these organisms, and provides additional evidence of taxa within these clades with potential preference for brackish environments, not just low salinity or marine.…”

The Arctic summer microbiome across Fram Strait: Depth, longitude, and substrate concentrations structure microbial diversity in the euphotic zone

“…Nitrosomonas (ammonia oxidizers) and LS-NOB (nitrite oxidizers) might perform shared denitrification (Lehtovirta-Morley, 2018), although probably less effective than ammonia oxidation by archaea (Rasmussen & Francis, 2022). AEGEAN-169 (recently designated as SAR11 clade V) can potentially utilize a broader range of CHOs than other SAR11 clades, and might participate in trace metal cycling and thiamin synthesis (Getz et al, 2023).…”