Mutualistic interaction between vitamin B-12 dependent algae and heterotrophic bacteria exhibit regulation

Environmental Microbiology (Impact Factor: 6.2). 03/2012; 14(6):1466 - 1476. DOI: 10.1111/j.1462-2920.2012.02733.x


Many algae are auxotrophs for vitamin B12 (cobalamin), which they need as a cofactor for B12-dependent methionine synthase (METH). Because only prokaryotes can synthesize the cobalamin, they must be the ultimate source of the vitamin. In the laboratory, a direct interaction between algae and heterotrophic bacteria has been shown, with bacteria supplying cobalamin in exchange for fixed carbon. Here we establish a system to study this interaction at the molecular level. In a culture of a B12-dependent green alga Chlamydomonas nivalis, we found a contaminating bacterium, identified by 16S rRNA analysis as Mesorhizobium sp. Using the sequenced strain of M. loti (MAFF303099), we found that it was able to support the growth of B12-dependent Lobomonas rostrata, another green alga, in return for fixed carbon. The two organisms form a stable equilibrium in terms of population numbers, which is maintained over many generations in semi-continuous culture, indicating a degree of regulation. However, addition of either vitamin B12 or a carbon source for the bacteria perturbs the equilibrium, demonstrating that the symbiosis is mutualistic and facultative. Chlamydomonas reinhardtii does not require B12 for growth because it encodes a B12-independent methionine synthase, METE, the gene for which is suppressed by addition of exogenous B12. Co-culturing C. reinhardtii with M. loti also results in reduction of METE expression, demonstrating that the bacterium can deliver the vitamin to this B12-independent alga. We discuss the implications of this for the widespread distribution of cobalamin auxotrophy in the algal kingdom.

  • Source
    • "Experimental evidence supports complementation of lost capabilities by non-specific interaction partners: a range of reduced sulfur sources can be used by SAR11 (Tripp et al., 2008) and many bacteria can provide B 12 for auxotrophs (Croft et al., 2005). Additionally, some obligate relationships, at least in artificial laboratory conditions, do not involve regulation or signaling (Durham et al., 2015), while others are regulated (Kazamia et al., 2012), suggesting a number of "
    [Show abstract] [Hide abstract]
    ABSTRACT: Microbes numerically dominate aquatic ecosystems and play key roles in the biogeochemistry and the health of these environments. Due to their short generations times and high diversity, microbial communities are among the first responders to environmental changes, including natural and anthropogenic disturbances such as storms, pollutant releases, and upwelling. These disturbances affect members of the microbial communities both directly and indirectly through interactions with impacted community members. Thus, interactions can influence disturbance propagation through the microbial community by either expanding the range of organisms affected or buffering the influence of disturbance. For example, interactions may expand the number of disturbance-affected taxa by favoring a competitor or buffer the impacts of disturbance when a potentially disturbance-responsive clade's growth is limited by an essential microbial partner. Here, we discuss the potential to use inferred ecological association networks to examine how disturbances propagate through microbial communities focusing on a case study of a coastal community's response to a storm. This approach will offer greater insight into how disturbances can produce community-wide impacts on aquatic environments following transient changes in environmental parameters.
    Full-text · Article · Oct 2015 · Frontiers in Microbiology
  • Source
    • "In some cases vitamin B 12 is known to originate from an epibiontic member of the Rhizobiales such as Rhizobium , Bradyrhizobium, or Mesorhizobium. For example, it has been demonstrated that the B 12 -dependent green flagellate Lobomonas rostrata obtains B 12 from a species of Mesorhizobium, and the alga provides the bacterium with fixed carbon in this mutualistic association (Kazamia et al. 2012). Likewise, the macroalga C. glomerata is known to require vitamin B 12 (Hoffman 1990), so it is reasonable to hypothesize that this host's microbiome would include taxa and genes associated with production of this vitamin. "
    [Show abstract] [Hide abstract]
    ABSTRACT: A recent perspective article ably argued that fully sequencing more algal genomes would enable progress in diverse areas of fundamental and applied studies. More algal genomes would add resources needed to build well-supported phylogenies, improve our understanding of how horizontal gene transfer has influenced the evolution of algal genomes, provide useful ecological insights, and generate information essential to manipulating the genomes of industrially useful algae (J. Phycol. 51:1). We agree that more algal genomes would be quite beneficial, and also propose that more algal metagenomes would enable progress in both predictable and unforeseen directions.
    Full-text · Article · Oct 2015 · Journal of Phycology
  • Source
    • "However, the prevalence of algal vitamin B 12 requirers in nature implies that there is a readily available/common niche for auxotrophic algae to occupy. Current understanding suggests that B 12 requirers may obtain a source of vitamin B 12 through: (i) direct interactions with heterotrophic bacteria (Croft et al., 2005; Wagner-Dö bler et al., 2010; Kazamia et al, 2012) and/or (ii) uptake from the dissolved vitamin pool, in patches of elevated microbial activity—that is, non-specific interactions with prokaryote producers (Karl, 2002; Azam and Malfatti, 2007). Based on genome analyses, prokaryotic taxa implicated in cobalamin synthesis include members of the Alphaproteobacteria, Gammaproteobacteria, Cyanobacteria and Bacteroidetes (Sañ udo-Wilhelmy et al., 2014). "
    [Show abstract] [Hide abstract]
    ABSTRACT: A widespread and complex distribution of vitamin requirements exists over the entire tree of life, with many species having evolved vitamin dependence, both within and between different lineages. Vitamin availability has been proposed to drive selection for vitamin dependence, in a process that links an organism's metabolism to the environment, but this has never been demonstrated directly. Moreover, understanding the physiological processes and evolutionary dynamics that influence metabolic demand for these important micronutrients has significant implications in terms of nutrient acquisition and, in microbial organisms, can affect community composition and metabolic exchange between coexisting species. Here we investigate the origins of vitamin dependence, using an experimental evolution approach with the vitamin B12-independent model green alga Chlamydomonas reinhardtii. In fewer than 500 generations of growth in the presence of vitamin B12, we observe the evolution of a B12-dependent clone that rapidly displaces its ancestor. Genetic characterization of this line reveals a type-II Gulliver-related transposable element integrated into the B12-independent methionine synthase gene (METE), knocking out gene function and fundamentally altering the physiology of the alga.The ISME Journal advance online publication, 19 December 2014; doi:10.1038/ismej.2014.230.
    Full-text · Article · Dec 2014 · The ISME Journal
Show more