Biology subjects

Biller, S.

Publications and source records attributed to Biller, S..

5 recordsLinked to original sources

bioRxiv2022

Marine viral particles reveal an expansive repertoire of phage-parasitizing mobile elements

Phage satellites are mobile genetic elements that propagate by parasitizing bacteriophage replication. We report here the discovery of abundant and diverse phage satellites that were packaged as concatemeric repeats within naturally occurring bacteriophage particles in seawater. These same phage-parasitizing mobile elements were found integrated in the genomes of dominant co-occurring bacterioplankton species. Like known phage satellites, many of the marine phage satellites encoded genes for integration, DNA replication, phage interference, and capsid assembly. Many also contained distinctive gene suites indicative of unique virus hijacking, phage interference and mobilization mechanisms. Marine phage satellite sequences were widespread in local and global oceanic virioplankton populations, reflecting their ubiquity, abundance, and temporal persistence in marine planktonic communities worldwide. Their gene content and putative life cycles suggest they may impact host-cell phage immunity and defense, lateral gene transfer, and bacteriophage-induced cell mortality and host and virus productivity. These previously unrecognized marine phage satellites therefore have potential to impact the ecology and evolution of bacteria and their bacteriophages in the ocean, and similar phage parasites likely thrive in many other microbial habitats as well. Significance statementPhage satellites are mobile genetic elements that parasitize bacteriophage, thereby exerting profound biological and ecological impacts. To date however, phage satellites have been found primarily in Gram-positive cocci and a few Gram-negative bacteria, many of which are human pathogens. Direct inspection of "wild" marine virus particles however, revealed that phage satellites are widely distributed in the sea, and that their genetic diversity, gene repertoires, and host ranges are much greater than previously supposed. Our analyses provide insight into their parasitic life cycles, potential satellite-helper-phage interactions, and reproductive strategies of these newly recognized phage-parasitizing mobile elements. Their properties, diversity and environmental distributions suggest they exert pervasive influence on marine plankton ecology and bacterial and virus evolution in the sea.

microbiology↗

bioRxiv2022

Environmental and taxonomic drivers of bacterial extracellular vesicle production in marine ecosystems

Extracellular vesicles are small ([~]50-250 nm diameter) membrane-bound structures released by cells into their surrounding environment. Vesicles are abundant in the global oceans and likely play a number of ecological roles in these microbially dominated ecosystems, yet we know nothing about what influences their production and distributions. Here we examine how vesicle production varies among different strains of cultivated marine microbes and explore the degree to which this is influenced by some key environmental variables. We show that vesicle production rates - the number of vesicles produced per cell per generation - vary across an order of magnitude in cultures of marine Proteobacteria, Cyanobacteria, and Bacteroidetes. Vesicle production rates further differ among strains of the cyanobacterium Prochlorococcus, and vary across temperature and light gradients. These data suggest that both community composition and local environmental conditions modulate the production and standing stock of vesicles in the oceans. Examining samples from the oligotrophic North Pacific Gyre, we show depth-dependent changes in the abundance of vesicle-like particles in the upper water column in a manner broadly consistent with culture observations: highest vesicle abundances are found near the surface, where light irradiances and temperatures are greatest, and then decrease with depth. This work represents the beginnings of a quantitative framework for describing extracellular vesicle dynamics in the oceans - essential as we begin to incorporate vesicles into our ecological and biogeochemical understanding of marine ecosystems. ImportanceBacteria secrete extracellular vesicles containing a wide variety of cellular compounds, including lipids, proteins, nucleic acids, and small molecules, into their surrounding environment. These structures are found in diverse microbial habitats, including the oceans, where their distributions vary throughout the water column. Differences in vesicle abundances likely affect their functional impacts within microbial ecosystems, but the factors influencing vesicle distributions in the environment remain poorly understood. Using quantitative analysis of marine microbial cultures, we show that bacterial vesicle production in the oceans is shaped by a combination of biotic and abiotic factors. Our data indicate that different marine taxa release vesicles at rates varying across an order of magnitude, and that vesicle production can change dynamically as a function of environmental conditions. Taken together with direct measurements of vesicle concentrations in the oceans, these culture-based measurements further provide a window into estimating vesicle loss rates. These findings represent a step forward in our understanding of marine vesicle distributions and provide a basis for quantitatively exploring vesicle dynamics in natural ecosystems.

microbiology↗

bioRxiv2021

Siderophores as an iron source for Prochlorococcus in deep chlorophyll maximum layers of the oligotrophic ocean

Prochlorococcus is one of the most abundant photosynthesizing organisms in the oligotrophic oceans. Gene content variation among Prochlorococcus populations in separate ocean basins often mirrors the selective pressures imposed by the regions distinct biogeochemistry. By pairing genomic datasets with trace metal concentrations from across the global ocean, we show that the genomic capacity for siderophore-mediated iron uptake is widespread in low-light adapted Prochlorococcus populations from iron-depleted regions of the oligotrophic Pacific and S. Atlantic oceans: Prochlorococcus siderophore consumers were absent in the N. Atlantic ocean (higher iron flux) but constituted up to half of all Prochlorococcus genomes from metagenomes in the N. Pacific (lower iron flux). Prochlorococcus siderophore consumers, like many other bacteria with this trait, also lack siderophore biosynthesis genes indicating that they scavenge exogenous siderophores from seawater. Statistical modeling suggests that the capacity for siderophore uptake is endemic to remote ocean regions where atmospheric iron fluxes are the smallest, particularly at deep chlorophyll maximum and primary nitrite maximum layers. We argue that abundant siderophore consumers at these two common oceanographic features could be a symptom of wider community iron stress, consistent with prior hypotheses. Our results provide a clear example of iron as a selective force driving the evolution of Prochlorococcus.

ecology↗

bioRxiv2020

Coping with darkness: The adaptive response of marine picocyanobacteria to repeated light energy deprivation

The picocyanobacteria Prochlorococcus and Synechococcus are found throughout the oceans euphotic zone, where the daily light:dark cycle drives their physiology. Periodic deep mixing events can, however, move cells below this zone, depriving them of light for extended periods of time. Here we demonstrate that Prochlorococcus and Synechococcus can adapt to tolerate repeated periods of light energy deprivation. Cyanobacterial cultures kept in the dark for 3 days and then returned to the light initially required 18-26 days to resume growth, but after multiple rounds of dark exposure the strains began to regrow after only 1-2 days. This dark-tolerant phenotype was stable and heritable; cultures retained the trait across at least 18-21 generations even when grown in a standard 13:11 light:dark cycle. We found no genetic differences between the dark-tolerant and parental strains of Prochlorococcus NATL2A, indicating that an epigenetic change is responsible for the adaptation. To begin to explore this possibility, we asked whether DNA methylation - an epigenetic mechanism in bacteria - occurs in Prochlorococcus. LC-MS/MS analysis showed that while DNA methylations, including 6mA and 5mC, are found in some other Prochlorococcus strains, no methylations were detected in either the parental or dark-tolerant strain used in our experiments -i.e. the NATL2A strain. These findings suggest that Prochlorococcus utilizes a yet-to-be-determined epigenetic mechanism to adapt to the stress of extended light energy deprivation.

microbiology↗

bioRxiv2020

Gene exchange networks define species-like units in marine prokaryotes

Post-submission note. Since the original submission of this manuscript to bioRxiv, we discovered that some of our results may be impacted by the limitations of some of the comparative genomics tools used in this study. We are working on a revised version of the manuscript. Although horizontal gene transfer is recognized as a major evolutionary process in Bacteria and Archaea, its general patterns remain elusive, due to difficulties tracking genes at relevant resolution and scale within complex microbiomes. To circumvent these challenges, we analyzed a randomized sample of >12,000 genomes of individual cells of Bacteria and Archaea in the tropical and subtropical ocean - a well-mixed, global environment. We found that marine microorganisms form gene exchange networks (GENs) within which transfers of both flexible and core genes are frequent, including the rRNA operon that is commonly used as a conservative taxonomic marker. The data revealed efficient gene exchange among genomes with <28% nucleotide difference, indicating that GENs are much broader lineages than the nominal microbial species, which are currently delineated at 4-6% nucleotide difference. The 42 largest GENs accounted for 90% of cells in the tropical ocean microbiome. Frequent gene exchange within GENs helps explain how marine microorganisms maintain millions of rare genes and adapt to a dynamic environment despite extreme genome streamlining of their individual cells. Our study suggests that sharing of pangenomes through horizontal gene transfer is a defining feature of fundamental evolutionary units in marine planktonic microorganisms and, potentially, other microbiomes.

microbiology↗