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Roseobacticides: small molecule modulators of an algal-bacterial symbiosis.

Seyedsayamdost MR, Carr G, Kolter R, Clardy J - J. Am. Chem. Soc. (2011)

Bottom Line: A recent study of Phaeobacter gallaeciensis, a member of the large roseobacter clade of α-proteobacteria, and Emiliania huxleyi, a prominent member of the microphytoplankton found in large algal blooms, revealed that an algal senescence signal produced by E. huxleyi elicits the production of novel algaecides, the roseobacticides, from the bacterial symbiont.Structures of the new family members arise from variable substituents at the C3 and C7 positions of the roseobacticide core as the diversifying elements and suggest that the roseobacticides result from modifications and combinations of aromatic amino acids.Together these studies support a model in which algal senescence converts a mutualistic bacterial symbiont into an opportunistic parasite of its hosts.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, Massachusetts 02115, United States.

ABSTRACT
Marine bacteria and microalgae engage in dynamic symbioses mediated by small molecules. A recent study of Phaeobacter gallaeciensis, a member of the large roseobacter clade of α-proteobacteria, and Emiliania huxleyi, a prominent member of the microphytoplankton found in large algal blooms, revealed that an algal senescence signal produced by E. huxleyi elicits the production of novel algaecides, the roseobacticides, from the bacterial symbiont. In this report, the generality of these findings are examined by expanding the number of potential elicitors. This expansion led to the identification of nine new members of the roseobacticide family, rare bacterial troponoids, which provide insights into both their biological roles and their biosynthesis. The qualitative and quantitative changes in the levels of roseobacticides induced by the additional elicitors and the elicitors' varied efficiencies support the concept of host-targeted roseobacticide production. Structures of the new family members arise from variable substituents at the C3 and C7 positions of the roseobacticide core as the diversifying elements and suggest that the roseobacticides result from modifications and combinations of aromatic amino acids. Together these studies support a model in which algal senescence converts a mutualistic bacterial symbiont into an opportunistic parasite of its hosts.

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Proposed model for the dynamic interaction between P. gallaeciensis B107 and E. huxleyi. The two phases of the interaction are shown by green (mutualistic phase) and red (parasitic phase) arrows. Compounds produced by P. gallaeciensis BS107 and E. huxleyi are shown in blue and gray, respectively. (A) Mutualistic phase of the symbiosis. Under these conditions, the healthy algal host provides DMSP (6) and an attachment surface, and the bacterial symbiont provides growth promoter 5 and the antibiotic tropodithietic acid (TDA, 3), which is biosynthesized from 5 via precursor 4.(7) (B) Parasitic phase of the symbiosis. When the algal host senesces, it releases pCA (7), which elicits the production of antialgal compounds, the roseobacticides (1, 2), likely derived from 5. Note that 5 is likely a precursor to metabolites that are health-promoting in the mutualistic phase (A) and toxic in the parasitic phase (B). Thus, 5 may be a critical player in the switch from mutualism to parasitism.
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fig1: Proposed model for the dynamic interaction between P. gallaeciensis B107 and E. huxleyi. The two phases of the interaction are shown by green (mutualistic phase) and red (parasitic phase) arrows. Compounds produced by P. gallaeciensis BS107 and E. huxleyi are shown in blue and gray, respectively. (A) Mutualistic phase of the symbiosis. Under these conditions, the healthy algal host provides DMSP (6) and an attachment surface, and the bacterial symbiont provides growth promoter 5 and the antibiotic tropodithietic acid (TDA, 3), which is biosynthesized from 5 via precursor 4.(7) (B) Parasitic phase of the symbiosis. When the algal host senesces, it releases pCA (7), which elicits the production of antialgal compounds, the roseobacticides (1, 2), likely derived from 5. Note that 5 is likely a precursor to metabolites that are health-promoting in the mutualistic phase (A) and toxic in the parasitic phase (B). Thus, 5 may be a critical player in the switch from mutualism to parasitism.

Mentions: Investigating the chemistry underlying microbial symbioses provides opportunities to discover new small molecules in the context of the biological roles they have evolved to fulfill.(1) In a recent example of this search strategy, we described roseobacticides A and B (Figure 1, 1, 2), which contain the previously unreported 1-oxaazulan-2-one core, and their ability to affect marine phytoplankton with nM potency.(2) The bacterial symbiosis partner, or symbiont, that produces these roseobacticides, Phaeobacter gallaeciensis BS107,(3) belongs to the roseobacter clade, a large, phylogenetically related group of marine α-proteobacteria that account for up to 25% of all bacteria in typical coastal communities.(4)P. gallaeciensis BS107 is easily cultured in the laboratory and under these conditions produces a number of secondary metabolites including the antibiotic tropodithietic acid (3), its precursor 4, and the plant growth promoter phenylacetic acid (5).5−8P. gallaeciensis BS107 associates with Emiliania huxleyi, a globally distributed single-celled microalga covered with ornate CaCO3 disks.2,9E. huxleyi is a major contributor (80–90%) to massive (104–105 km2) seasonal algal blooms that are easily visible in satellite images, and it, along with other microphytoplankton, produces nearly half of the Earth’s atmospheric oxygen.(10) In addition to fixing CO2 through photosynthesis, E. huxleyi sequesters CO2 in the CaCO3 disks that surround each algal cell, and also plays a role in the global sulfur cycle by reducing dissolved sulfate to methionine, cysteine, and dimethylsulfoniopropionate (DMSP, 6).(11) DMSP attracts roseobacter (and other) bacteria, which use it as a carbon and sulfur source.(12) The bacteria can metabolize DMSP to volatile DMS, which in the atmosphere is converted to condensation nuclei for water droplets.4,13 Thus, roseobacter-microalgal symbioses play key roles in important biogeochemical processes.4,14


Roseobacticides: small molecule modulators of an algal-bacterial symbiosis.

Seyedsayamdost MR, Carr G, Kolter R, Clardy J - J. Am. Chem. Soc. (2011)

Proposed model for the dynamic interaction between P. gallaeciensis B107 and E. huxleyi. The two phases of the interaction are shown by green (mutualistic phase) and red (parasitic phase) arrows. Compounds produced by P. gallaeciensis BS107 and E. huxleyi are shown in blue and gray, respectively. (A) Mutualistic phase of the symbiosis. Under these conditions, the healthy algal host provides DMSP (6) and an attachment surface, and the bacterial symbiont provides growth promoter 5 and the antibiotic tropodithietic acid (TDA, 3), which is biosynthesized from 5 via precursor 4.(7) (B) Parasitic phase of the symbiosis. When the algal host senesces, it releases pCA (7), which elicits the production of antialgal compounds, the roseobacticides (1, 2), likely derived from 5. Note that 5 is likely a precursor to metabolites that are health-promoting in the mutualistic phase (A) and toxic in the parasitic phase (B). Thus, 5 may be a critical player in the switch from mutualism to parasitism.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3211371&req=5

fig1: Proposed model for the dynamic interaction between P. gallaeciensis B107 and E. huxleyi. The two phases of the interaction are shown by green (mutualistic phase) and red (parasitic phase) arrows. Compounds produced by P. gallaeciensis BS107 and E. huxleyi are shown in blue and gray, respectively. (A) Mutualistic phase of the symbiosis. Under these conditions, the healthy algal host provides DMSP (6) and an attachment surface, and the bacterial symbiont provides growth promoter 5 and the antibiotic tropodithietic acid (TDA, 3), which is biosynthesized from 5 via precursor 4.(7) (B) Parasitic phase of the symbiosis. When the algal host senesces, it releases pCA (7), which elicits the production of antialgal compounds, the roseobacticides (1, 2), likely derived from 5. Note that 5 is likely a precursor to metabolites that are health-promoting in the mutualistic phase (A) and toxic in the parasitic phase (B). Thus, 5 may be a critical player in the switch from mutualism to parasitism.
Mentions: Investigating the chemistry underlying microbial symbioses provides opportunities to discover new small molecules in the context of the biological roles they have evolved to fulfill.(1) In a recent example of this search strategy, we described roseobacticides A and B (Figure 1, 1, 2), which contain the previously unreported 1-oxaazulan-2-one core, and their ability to affect marine phytoplankton with nM potency.(2) The bacterial symbiosis partner, or symbiont, that produces these roseobacticides, Phaeobacter gallaeciensis BS107,(3) belongs to the roseobacter clade, a large, phylogenetically related group of marine α-proteobacteria that account for up to 25% of all bacteria in typical coastal communities.(4)P. gallaeciensis BS107 is easily cultured in the laboratory and under these conditions produces a number of secondary metabolites including the antibiotic tropodithietic acid (3), its precursor 4, and the plant growth promoter phenylacetic acid (5).5−8P. gallaeciensis BS107 associates with Emiliania huxleyi, a globally distributed single-celled microalga covered with ornate CaCO3 disks.2,9E. huxleyi is a major contributor (80–90%) to massive (104–105 km2) seasonal algal blooms that are easily visible in satellite images, and it, along with other microphytoplankton, produces nearly half of the Earth’s atmospheric oxygen.(10) In addition to fixing CO2 through photosynthesis, E. huxleyi sequesters CO2 in the CaCO3 disks that surround each algal cell, and also plays a role in the global sulfur cycle by reducing dissolved sulfate to methionine, cysteine, and dimethylsulfoniopropionate (DMSP, 6).(11) DMSP attracts roseobacter (and other) bacteria, which use it as a carbon and sulfur source.(12) The bacteria can metabolize DMSP to volatile DMS, which in the atmosphere is converted to condensation nuclei for water droplets.4,13 Thus, roseobacter-microalgal symbioses play key roles in important biogeochemical processes.4,14

Bottom Line: A recent study of Phaeobacter gallaeciensis, a member of the large roseobacter clade of α-proteobacteria, and Emiliania huxleyi, a prominent member of the microphytoplankton found in large algal blooms, revealed that an algal senescence signal produced by E. huxleyi elicits the production of novel algaecides, the roseobacticides, from the bacterial symbiont.Structures of the new family members arise from variable substituents at the C3 and C7 positions of the roseobacticide core as the diversifying elements and suggest that the roseobacticides result from modifications and combinations of aromatic amino acids.Together these studies support a model in which algal senescence converts a mutualistic bacterial symbiont into an opportunistic parasite of its hosts.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, Massachusetts 02115, United States.

ABSTRACT
Marine bacteria and microalgae engage in dynamic symbioses mediated by small molecules. A recent study of Phaeobacter gallaeciensis, a member of the large roseobacter clade of α-proteobacteria, and Emiliania huxleyi, a prominent member of the microphytoplankton found in large algal blooms, revealed that an algal senescence signal produced by E. huxleyi elicits the production of novel algaecides, the roseobacticides, from the bacterial symbiont. In this report, the generality of these findings are examined by expanding the number of potential elicitors. This expansion led to the identification of nine new members of the roseobacticide family, rare bacterial troponoids, which provide insights into both their biological roles and their biosynthesis. The qualitative and quantitative changes in the levels of roseobacticides induced by the additional elicitors and the elicitors' varied efficiencies support the concept of host-targeted roseobacticide production. Structures of the new family members arise from variable substituents at the C3 and C7 positions of the roseobacticide core as the diversifying elements and suggest that the roseobacticides result from modifications and combinations of aromatic amino acids. Together these studies support a model in which algal senescence converts a mutualistic bacterial symbiont into an opportunistic parasite of its hosts.

Show MeSH
Related in: MedlinePlus