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  1. Rappe, Michael S. (Ed.)
    ABSTRACT For the abundant marine Alphaproteobacterium Pelagibacter (SAR11), and other bacteria, phages are powerful forces of mortality. However, little is known about the most abundant Pelagiphages in nature, such as the widespread HTVC023P-type, which is currently represented by two cultured phages. Using viral metagenomic data sets and fluorescence-activated cell sorting, we recovered 80 complete, undescribed Podoviridae genomes that form 10 phylogenomically distinct clades (herein, named Clades I to X) related to the HTVC023P-type. These expanded the HTVC023P-type pan-genome by 15-fold and revealed 41 previously unknown auxiliary metabolic genes (AMGs) in this viral lineage. Numerous instances of partner-AMGs (colocated and involved in related functions) were observed, including partners in nucleotide metabolism, DNA hypermodification, and Curli biogenesis. The Type VIII secretion system (T8SS) responsible for Curli biogenesis was identified in nine genomes and expanded the repertoire of T8SS proteins reported thus far in viruses. Additionally, the identified T8SS gene cluster contained an iron-dependent regulator (FecR), as well as a histidine kinase and adenylate cyclase that can be implicated in T8SS function but are not within T8SS operons in bacteria. While T8SS are lacking in known Pelagibacter , they contribute to aggregation and biofilm formation in other bacteria. Phylogenetic reconstructions of partner-AMGs indicate derivation from cellular lineages with a more recent transfer between viral families. For example, homologs of all T8SS genes are present in syntenic regions of distant Myoviridae Pelagiphages, and they appear to have alphaproteobacterial origins with a later transfer between viral families. The results point to an unprecedented multipartner-AMG transfer between marine Myoviridae and Podoviridae. Together with the expansion of known metabolic functions, our studies provide new prospects for understanding the ecology and evolution of marine phages and their hosts. IMPORTANCE One of the most abundant and diverse marine bacterial groups is Pelagibacter . Phages have roles in shaping Pelagibacter ecology; however, several Pelagiphage lineages are represented by only a few genomes. This paucity of data from even the most widespread lineages has imposed limits on the understanding of the diversity of Pelagiphages and their impacts on hosts. Here, we report 80 complete genomes, assembled directly from environmental data, which are from undescribed Pelagiphages and render new insights into the manipulation of host metabolism during infection. Notably, the viruses have functionally related partner genes that appear to be transferred between distant viruses, including a suite that encode a secretion system which both brings a new functional capability to the host and is abundant in phages across the ocean. Together, these functions have important implications for phage evolution and for how Pelagiphage infection influences host biology in manners extending beyond canonical viral lysis and mortality. 
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  2. Rappe, Michael S. (Ed.)
    ABSTRACT Bacterial biodegradation is a significant contributor to remineralization of polycyclic aromatic hydrocarbons (PAHs)—toxic and recalcitrant components of crude oil as well as by-products of partial combustion chronically introduced into seawater via atmospheric deposition. The Deepwater Horizon oil spill demonstrated the speed at which a seed PAH-degrading community maintained by chronic inputs responds to acute pollution. We investigated the diversity and functional potential of a similar seed community in the chronically polluted Port of Los Angeles (POLA), using stable isotope probing with naphthalene, deep-sequenced metagenomes, and carbon incorporation rate measurements at the port and in two sites in the San Pedro Channel. We demonstrate the ability of the community of degraders at the POLA to incorporate carbon from naphthalene, leading to a quick shift in microbial community composition to be dominated by the normally rare Colwellia and Cycloclasticus . We show that metagenome-assembled genomes (MAGs) belonged to these naphthalene degraders by matching their 16S-rRNA gene with experimental stable isotope probing data. Surprisingly, we did not find a full PAH degradation pathway in those genomes, even when combining genes from the entire microbial community, leading us to hypothesize that promiscuous dehydrogenases replace canonical naphthalene degradation enzymes in this site. We compared metabolic pathways identified in 29 genomes whose abundance increased in the presence of naphthalene to generate genomic-based recommendations for future optimization of PAH bioremediation at the POLA, e.g., ammonium as opposed to urea, heme or hemoproteins as an iron source, and polar amino acids. IMPORTANCE Oil spills in the marine environment have a devastating effect on marine life and biogeochemical cycles through bioaccumulation of toxic hydrocarbons and oxygen depletion by hydrocarbon-degrading bacteria. Oil-degrading bacteria occur naturally in the ocean, especially where they are supported by chronic inputs of oil or other organic carbon sources, and have a significant role in degradation of oil spills. Polycyclic aromatic hydrocarbons are the most persistent and toxic component of crude oil. Therefore, the bacteria that can break those molecules down are of particular importance. We identified such bacteria at the Port of Los Angeles (POLA), one of the busiest ports worldwide, and characterized their metabolic capabilities. We propose chemical targets based on those analyses to stimulate the activity of these bacteria in case of an oil spill in the Port POLA. 
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