Host population diversity as a driver of viral infection cycle in wild populations of green sulfur bacteria with long standing virus-host interactions

AbstractTemperate phages are viruses of bacteria that can establish two types of infection: a lysogenic infection in which the virus replicates with the host cell without producing virions, and a lytic infection where the host cell is eventually destroyed, and new virions are released. While both lytic and lysogenic infections are routinely observed in the environment, the ecological and evolutionary processes regulating these viral dynamics are still not well understood, especially for uncultivated virus-host pairs. Here, we characterized the long-term dynamics of uncultivated viruses infecting green sulfur bacteria (GSB) in a model freshwater lake (Trout Bog Lake, TBL). As no GSB virus has been formally described yet, we first used two complementary approaches to identify new GSB viruses from TBL; one in vitro based on flow cytometry cell sorting, the other in silico based on CRISPR spacer sequences. We then took advantage of existing TBL metagenomes covering the 2005–2018 period to examine the interactions between GSB and their viruses across years and seasons. From our data, GSB populations in TBL were constantly associated with at least 2-8 viruses each, including both lytic and temperate phages. The dominant GSB population in particular was consistently associated with two prophages with a nearly 100% infection rate for >10 years. We illustrate with a theoretical model that such an interaction can be stable given a low, but persistent, level of prophage induction in low-diversity host populations. Overall, our data suggest that lytic and lysogenic viruses can readily co-infect the same host population, and that host strain-level diversity might be an important factor controlling virus-host dynamics including lytic/lysogeny switch.

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Host population diversity as a driver of viral infection cycle in wild populations of green sulfur bacteria with long standing virus-host interactions

10.1101/2020.03.05.979559 ◽

2020 ◽

Cited By ~ 1

Author(s):

Maureen Berg ◽

Danielle Goudeau ◽

Charles Olmsted ◽

Katherine D McMahon ◽

Jennifer Thweatt ◽

...

Keyword(s):

Viral Infections ◽

Natural Populations ◽

Latency Period ◽

Green Sulfur Bacteria ◽

Host Population ◽

Population Diversity ◽

Infection Model ◽

Sulfur Bacteria ◽

Green Sulfur

ABSTRACTViral infections of bacterial hosts range from highly lytic to lysogenic, where highly lytic viruses undergo viral replication and immediately lyse their hosts, and lysogenic viruses have a latency period before replication and host lysis. While both types of infections are routinely observed in the environment, the ecological and evolutionary processes that regulate these different viral dynamics are still not well understood. In this study, we identify and characterize the long-term dynamics of uncultivated viruses infecting green sulfur bacteria (GSB) in a model freshwater lake sampled from 2005-2018. Because of the additional requirements for the laboratory cultivation of anaerobes like GSB, viruses infecting GSB have yet to be formally identified, leaving their diversity and impact on natural populations of GSB virtually unknown. In this study, we used two approaches to identify viruses infecting GSB; one in vitro based on flow cytometry cell sorting, the other in silico based on CRISPR spacer sequences. We then took advantage of existing bulk metagenomes derived from Trout Bog Lake covering the 2005-2018 period to examine the interactions between GSB hosts and their viruses across multiple years and seasons. From our data, GSB populations in Trout Bog Lake were found to be concurrently infected with at least 2-8 viruses each, many of which were lysogenic viruses; one GSB host population in particular was consistently associated with two lysogens with a nearly 100% infection rate for over 10 years. We illustrate with a theoretical infection model that such an interaction can be stable over multiple years given a low, but persistent level of lysogen induction in host populations with already high infection rates. Overall, our data suggest that single GSB populations are typically infected by multiple viruses at the same time, that lytic and lysogenic viruses can readily co-infect the same host population in the same ecosystem, and that host strain-level diversity might be an important factor controlling the lytic/lysogeny switch.

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In vitro activity of C-20 methyltransferase, BchU, involved in bacteriochlorophyllcbiosynthetic pathway in green sulfur bacteria

FEBS Letters ◽

10.1016/j.febslet.2005.01.087 ◽

2005 ◽

Vol 579 (9) ◽

pp. 1983-1987 ◽

Cited By ~ 22

Author(s):

Jiro Harada ◽

Yoshitaka Saga ◽

Yuki Yaeda ◽

Hirozo Oh-oka ◽

Hitoshi Tamiaki

Keyword(s):

Green Sulfur Bacteria ◽

Vitro Activity ◽

In Vitro Activity ◽

Sulfur Bacteria ◽

Green Sulfur

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In vitro stereospecific hydration activities of the 3-vinyl group of chlorophyll derivatives by BchF and BchV enzymes involved in bacteriochlorophyll c biosynthesis of green sulfur bacteria

Photosynthesis Research ◽

10.1007/s11120-016-0220-7 ◽

2016 ◽

Vol 130 (1-3) ◽

pp. 33-45 ◽

Cited By ~ 10

Author(s):

Misato Teramura ◽

Jiro Harada ◽

Hitoshi Tamiaki

Keyword(s):

Green Sulfur Bacteria ◽

Bacteriochlorophyll C ◽

Sulfur Bacteria ◽

Green Sulfur ◽

Vinyl Group ◽

Chlorophyll Derivatives

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Origin and Evolution of Photosystems: Lessons from Green Sulfur Bacteria

ChemPhotoChem ◽

10.1002/cptc.202100019 ◽

2021 ◽

Author(s):

Guillaume Tcherkez ◽

Nicolas Papon

Keyword(s):

Green Sulfur Bacteria ◽

Origin And Evolution ◽

Sulfur Bacteria ◽

Green Sulfur

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Novel green sulfur bacteria phylotypes detected in saline environments: ecophysiological characters versus phylogenetic taxonomy

Antonie van Leeuwenhoek ◽

10.1007/s10482-010-9420-x ◽

2010 ◽

Vol 97 (4) ◽

pp. 419-431

Author(s):

Xavier Triadó-Margarit ◽

Xavier Vila ◽

Charles A. Abella

Keyword(s):

Green Sulfur Bacteria ◽

Saline Environments ◽

Phylogenetic Taxonomy ◽

Sulfur Bacteria ◽

Green Sulfur

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Plasmodium knowlesi: a relevant, versatile experimental malaria model

Parasitology ◽

10.1017/s0031182016002286 ◽

2016 ◽

Vol 145 (1) ◽

pp. 56-70 ◽

Cited By ~ 8

Author(s):

ERICA M. PASINI ◽

ANNE-MARIE ZEEMAN ◽

ANNEMARIE VOORBERG-VAN DER WEL ◽

CLEMENS H. M. KOCKEN

Keyword(s):

Parasite Species ◽

Vaccine Development ◽

Plasmodium Knowlesi ◽

Host Interactions ◽

Model Studies ◽

Human Red Blood Cells ◽

Malaria Model ◽

Human Primate

SUMMARYThe primate malariaPlasmodium knowlesihas a long-standing history as an experimental malaria model. Studies using this model parasite in combination with its various natural and experimental non-human primate hosts have led to important advances in vaccine development and in our understanding of malaria invasion, immunology and parasite–host interactions. The adaptation to long-termin vitrocontinuous blood stage culture in rhesus monkey,Macaca fascicularisand human red blood cells, as well as the development of various transfection methodologies has resulted in a highly versatile experimental malaria model, further increasing the potential of what was already a very powerful model. The growing evidence thatP. knowlesiis an important human zoonosis in South-East Asia has added relevance to former and future studies of this parasite species.

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Signature pigments of green sulfur bacteria in lower Pleistocene deposits from the Banyoles lacustrine area (Spain)

Journal of Paleolimnology ◽

10.1007/s10933-005-3731-3 ◽

2005 ◽

Vol 34 (2) ◽

pp. 271-280 ◽

Cited By ~ 16

Author(s):

N. Mallorquí ◽

J.B. Arellano ◽

C.M. Borrego ◽

L.J. Garcia-Gil

Keyword(s):

Green Sulfur Bacteria ◽

Sulfur Bacteria ◽

Lower Pleistocene ◽

Green Sulfur

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Differential RNA Sequencing Implicates Sulfide as the Master Regulator of S 0 Metabolism in Chlorobaculum tepidum and Other Green Sulfur Bacteria

Applied and Environmental Microbiology ◽

10.1128/aem.01966-17 ◽

2017 ◽

Vol 84 (3) ◽

Cited By ~ 1

Author(s):

Jacob M. Hilzinger ◽

Vidhyavathi Raman ◽

Kevin E. Shuman ◽

Brian J. Eddie ◽

Thomas E. Hanson

Keyword(s):

Gene Expression ◽

Elemental Sulfur ◽

Green Sulfur Bacteria ◽

Electron Donors ◽

Reduced Sulfur Compounds ◽

Promoter Elements ◽

Content Type ◽

Sulfur Bacteria ◽

Chlorobaculum Tepidum ◽

Green Sulfur

ABSTRACT The green sulfur bacteria ( Chlorobiaceae ) are anaerobes that use electrons from reduced sulfur compounds (sulfide, S 0 , and thiosulfate) as electron donors for photoautotrophic growth. Chlorobaculum tepidum , the model system for the Chlorobiaceae , both produces and consumes extracellular S 0 globules depending on the availability of sulfide in the environment. These physiological changes imply significant changes in gene regulation, which has been observed when sulfide is added to Cba. tepidum growing on thiosulfate. However, the underlying mechanisms driving these gene expression changes, i.e., the specific regulators and promoter elements involved, have not yet been defined. Here, differential RNA sequencing (dRNA-seq) was used to globally identify transcript start sites (TSS) that were present during growth on sulfide, biogenic S 0 , and thiosulfate as sole electron donors. TSS positions were used in combination with RNA-seq data from cultures growing on these same electron donors to identify both basal promoter elements and motifs associated with electron donor-dependent transcriptional regulation. These motifs were conserved across homologous Chlorobiaceae promoters. Two lines of evidence suggest that sulfide-mediated repression is the dominant regulatory mode in Cba. tepidum . First, motifs associated with genes regulated by sulfide overlap key basal promoter elements. Second, deletion of the Cba. tepidum 1277 ( CT1277 ) gene, encoding a putative regulatory protein, leads to constitutive overexpression of the sulfide:quinone oxidoreductase CT1087 in the absence of sulfide. The results suggest that sulfide is the master regulator of sulfur metabolism in Cba. tepidum and the Chlorobiaceae . Finally, the identification of basal promoter elements with differing strengths will further the development of synthetic biology in Cba. tepidum and perhaps other Chlorobiaceae . IMPORTANCE Elemental sulfur is a key intermediate in biogeochemical sulfur cycling. The photoautotrophic green sulfur bacterium Chlorobaculum tepidum either produces or consumes elemental sulfur depending on the availability of sulfide in the environment. Our results reveal transcriptional dynamics of Chlorobaculum tepidum on elemental sulfur and increase our understanding of the mechanisms of transcriptional regulation governing growth on different reduced sulfur compounds. This report identifies genes and sequence motifs that likely play significant roles in the production and consumption of elemental sulfur. Beyond this focused impact, this report paves the way for the development of synthetic biology in Chlorobaculum tepidum and other Chlorobiaceae by providing a comprehensive identification of promoter elements for control of gene expression, a key element of strain engineering.

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Rapid evolution of decreased host susceptibility drives a stable relationship between ultrasmall parasite TM7x and its bacterial host

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1810625115 ◽

2018 ◽

Vol 115 (48) ◽

pp. 12277-12282 ◽

Cited By ~ 18

Author(s):

Batbileg Bor ◽

Jeffrey S. McLean ◽

Kevin R. Foster ◽

Lujia Cen ◽

Thao T. To ◽

...

Keyword(s):

Host Cell ◽

Rapid Evolution ◽

Host Population ◽

Host Cells ◽

Host Susceptibility ◽

Bacterial Host ◽

Narrow Host Range ◽

Stable Relationship ◽

Candidate Phyla Radiation

Around one-quarter of bacterial diversity comprises a single radiation with reduced genomes, known collectively as the Candidate Phyla Radiation. Recently, we coisolated TM7x, an ultrasmall strain of the Candidate Phyla Radiation phylum Saccharibacteria, with its bacterial host Actinomyces odontolyticus strain XH001 from human oral cavity and stably maintained as a coculture. Our current work demonstrates that within the coculture, TM7x cells establish a long-term parasitic association with host cells by infecting only a subset of the population, which stay viable yet exhibit severely inhibited cell division. In contrast, exposure of a naïve A. odontolyticus isolate, XH001n, to TM7x cells leads to high numbers of TM7x cells binding to each host cell, massive host cell death, and a host population crash. However, further passaging reveals that XH001n becomes less susceptible to TM7x over time and enters a long-term stable relationship similar to that of XH001. We show that this reduced susceptibility is driven by rapid host evolution that, in contrast to many forms of phage resistance, offers only partial protection. The result is a stalemate where infected hosts cannot shed their parasites; nevertheless, parasite load is sufficiently low that the host population persists. Finally, we show that TM7x can infect and form stable long-term relationships with other species in a single clade of Actinomyces, displaying a narrow host range. This system serves as a model to understand how parasitic bacteria with reduced genomes such as those of the Candidate Phyla Radiation have persisted with their hosts and ultimately expanded in their diversity.

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