Comparison of Growth Rates of Aerobic Anoxygenic Phototrophic Bacteria and Other Bacterioplankton Groups in Coastal Mediterranean Waters

Abstract

Growth is one of the basic attributes of any living organism. Surprisingly, the growth rates of marine bacterioplankton are only poorly known. Current data suggest that marine bacteria grow relatively slowly, having generation times of several days. However, some bacterial groups, such as the aerobic anoxygenic phototrophic (AAP) bacteria, have been shown to grow much faster. Two manipulation experiments, in which grazing, viruses, and resource competition were reduced, were conducted in the coastal Mediterranean Sea (Blanes Bay Microbial Observatory). The growth rates of AAP bacteria and of several important phylogenetic groups (the Bacteroidetes, the alphaproteobacterial groups Roseobacter and SAR11, and the Gammaproteobacteria group and its subgroups the Alteromonadaceae and the NOR5/OM60 clade) were calculated from changes in cell numbers in the manipulation treatments. In addition, we examined the role that top-down (mortality due to grazers and viruses) and bottom-up (resource availability) factors play in determining the growth rates of these groups. Manipulations resulted in an increase of the growth rates of all groups studied, but its extent differed largely among the individual treatments and among the different groups. Interestingly, higher growth rates were found for the AAP bacteria (up to 3.71 day ؊1 ) and for the Alteromonadaceae (up to 5.44 day ؊1 ), in spite of the fact that these bacterial groups represented only a very low percentage of the total prokaryotic community. In contrast, the SAR11 clade, which was the most abundant group, was the slower grower in all treatments. Our results show that, in general, the least abundant groups exhibited the highest rates, whereas the most abundant groups were those growing more slowly, indicating that some minor groups, such the AAP bacteria, very likely contribute much more to the recycling of organic matter in the ocean than what their abundances alone would predict.The structure of bacterioplankton communities is defined by the type of organisms and by their relative proportions. Marine surface waters are typically composed of a few abundant groups, generally members of the Alphaproteobacteria and Gammaproteobacteria and the phylum Bacteroidetes (17), and many low-abundant taxa (32). The sizes of the different populations depend to a large extent on their growth rates, which can range from organisms that are almost inactive or dormant to cells growing very rapidly (12). In addition to the differences in activity between individual cells (40), recent evidence suggests that variability among different bacterioplankton groups also occurs (42,44,45). Since actively growing bacteria are responsible for major carbon and nutrient transformations in the ocean, determining the growth rates of individual groups is critical to understand their ecological roles and specific contributions to marine biogeochemical cycles.One of the groups that has been reported to grow at high rates in the ocean is the aerobic anoxygenic phototrophic (AAP) bacteria, which are phot...

Expression patterns reveal niche diversification in a marine microbial assemblage

“…SE45, P. parvula Ellin514) and that the most abundant groups were not the most active (for example, SAR11 clade members). This is consistent with recent data on estuarine bacterioplankton 16S rRNA:DNA ratios (Campbell et al, 2011) and dilution experiments (Ferrera et al, 2011). The assumption that bacteria capable of rapid growth show this ability only intermittently under conditions that are conducive for blooming (Yooseph et al, 2010) may therefore underestimate the trophic and biogeochemical influence of these fast-growing taxa.…”

“…The assumption that bacteria capable of rapid growth show this ability only intermittently under conditions that are conducive for blooming (Yooseph et al, 2010) may therefore underestimate the trophic and biogeochemical influence of these fast-growing taxa. Instead, numbers may be kept in check by top-down control within the microbial food web (Worden et al, 2006;Ferrera et al, 2011). Selective bacterial mortality mediated through protist grazing or viral lysis (Suttle, 2007) would lessen competitive exclusion between co-occurring heterotrophs.…”

Global-scale distributions of marine surface bacterioplankton groups along gradients of salinity, temperature, and chlorophyll: a meta-analysis of fluorescence in situ hybridization studies

“…by Yoko kawa & Nagata (2005) in western North Pacific coastal waters and by Ferrera et al (2011) in Blanes Bay, who measured lower growth rates of the more abundant groups such as Alphaproteo bacteria, relative to less abundant but fastergrowing Bacteroidetes and Gammaproteobacteria. Ferrera et al (2011) ex perimentally showed that even though SAR11 was the most abundant bacterial group, it was also the one with the slowest growth. This links to our findings of weak relationships between Alphaproteobacteria and SAR11 abundance with chl a in coastal ecosystems in comparison to their importance in terms of contribution to BCS.…”

“…Indeed, evidence for different patterns in the control of bacterial community com-positions linked to differential growth and mortality grazing rates among the major bacterial groups was revealed e.g. by Yoko kawa & Nagata (2005) in western North Pacific coastal waters and by Ferrera et al (2011) in Blanes Bay, who measured lower growth rates of the more abundant groups such as Alphaproteo bacteria, relative to less abundant but fastergrowing Bacteroidetes and Gammaproteobacteria. Ferrera et al (2011) ex perimentally showed that even though SAR11 was the most abundant bacterial group, it was also the one with the slowest growth.…”

Synergistic effects of UVR and simulated stratification on commensalistic phytoplankton–bacteria relationship in two optically contrasting oligotrophic Mediterranean lakes

“…Moreover, the increased HBP found after exposure of samples to higher PAR intensity in the upper layers is consistent with the previously reported stimulatory effect of PAR on HBP (Morán et al, 2001;Medina-Sánchez et al, 2002;Pakulski et al, 2007). Furthermore, a potential presence of aerobic anoxygenic phototrophic bacteria (Bertoni et al, 2011;Mašín et al, 2012;Ferrara et al, 2011) should not be ruled out in accounting for the increased HBP under high PAR in the low-UVR lake.…”