Mortality by ribosomal sequencing (MoRS) provides a window into taxon-specific cell lysis

Abstract

Microbes are by far the dominant biomass in the world’s oceans and drive biogeochemical cycles that are critical to life on Earth. The composition of marine microbial communities is highly dynamic, spatially and temporally, with consequent effects on their functional roles. In part, these changes in composition result from viral lysis, which is taxon-specific and estimated to account for about half of marine microbial mortality. Here, we show that extracellular ribosomal RNA (rRNAext) is produced by viral lysis, and that specific lysed populations can be identified by sequencing rRNAext recovered from seawater samples. In ten seawater samples collected at five depths between the surface and 265 m during and following a phytoplankton bloom, lysis was detected in about 15% of 16,946 prokaryotic taxa, identified from amplicon sequence variants (ASVs), with lysis occurring in up to 34% of taxa within a water sample. The ratio of rRNAext to cellular rRNA (rRNAcell) was used as an index of taxon-specific lysis, and revealed that higher relative lysis was most commonly associated with copiotrophic bacteria that were in relatively low abundance, such as those in the genera Escherichia and Shigella spp., as well as members of the Bacteriodetes; whereas, relatively low lysis was more common in taxa that are often relatively abundant, such as members of the Pelagibacterales (i.e., SAR11 clade), cyanobacteria in the genus Synechococcus, and members of the phylum Thaumarchaeota (synonym, Nitrososphaerota) that comprised about 13–15% of the 16 S rRNA gene sequences below 30 m. These results provide an explanation for the long-standing conundrum of why highly productive bacteria that are readily isolated from seawater are often in very low abundance. The ability to estimate taxon-specific cell lysis will help explore the distribution and abundance of microbial populations in nature.

Contrasting drivers of abundant phage and prokaryotic communities in tropical, coastal ecosystems across the Isthmus of Panama

“…In contrast, variation in the prokaryotic communities was primarily driven by Synechococcus bacteria (top 3 most influential; Supplementary Dataset 5), which follows its known distinction between pelagic and coastal conditions 29 , such as the TEP between TWA here. The elevated importance of phages predicted to infect chemoheterotrophic in driving phage community composition compared to the elevated importance of photoautotrophic bacteria in driving prokaryotic community composition further highlights that phage lysis predominantly occurs on the most productive members of the community, which are often heterotrophic bacteria that experience boom-and-bust cycles as nutrients become available 28 .…”

“…These genera are known as dominant members of the ocean 26,27 ; furthermore, because the phage sequences may also correspond to integrated phages of the prokaryotic community, this may have resulted in the co-prevalence of these genera in both phage and prokaryotic communities. Nevertheless, the general lack of overlap in prevalent phage and prokaryotic genera may have resulted from several factors such as technical limitations in classifying both the phages and prokaryotic sequences or that most viral lysis occurs for rare but highly productive microbes, as has been observed off the coast of British Columbia in Canada 28 , which would result in dominant viruses that infect rarer hosts.…”

“…Very few of the most dominant phage members infect genera of the most dominant prokaryotes. This may be because most phages are infecting the most productive prokaryotes which exhibit boom and bust reproductive cycles, rather than the most stably abundant 28 . This infection pattern would support the popular phage-host interaction model, the Kill-the-Winner model, in which phages rise in abundance to kill the most dominant prokaryotes 44 .…”

Complete Genome Sequence of Vibrio natriegens Strain PWH3a

“… Vibrio natriegens strain PWH3a was isolated in 1989 by swabbing seawater collected from the research pier in Aransas Pass at The University of Texas at Austin, Marine Science Institute (27.8380 N, 97.0504 W) onto CPM seawater plates (0.05% Casamino Acids, 0.05% Peptone and 1% agar in filtered seawater) ( 1 , 2 ). Used as a model organism to study viruses in marine systems, mechanisms of viral decay, and iron sequestration ( 1 – 15 ), isolate PWH3a was initially described as V. natriegens strain PWH3a ( 3 ) and later as Vibrio alginolyticus strain PWH3a ( 13 , 14 ), based on partial 16S rRNA gene sequences. Here, we report that analysis of the complete genome firmly places strain PWH3a as an isolate of Vibrio natriegens .…”

Productive viral infections in oligotrophic marine waters

“…Our data shows that Gammaproteobacteria and Alphaproteobacteria are overrepresented among bMAGs undergoing viral infections, while cyanobacteria had low infection rates compared with their overall abundances. These results are consistent with a previous study in coastal seawater environments showing an overrepresentation of free rRNA (interpreted as recently lysed cells) from copiotrophic and low-abundance bacteria, such as those in the genera Escherichia and Shigella spp., as well as members of the Bacteriodetes (Zhong et al, 2022).…”