Natural Assemblages of Marine Proteobacteria and Members of the Cytophaga-Flavobacter Cluster Consuming Low- and High-Molecular-Weight Dissolved Organic Matter

Abstract

We used a method that combines microautoradiography with hybridization of fluorescent rRNA-targeted oligonucleotide probes to whole cells (MICRO-FISH) to test the hypothesis that the relative contributions of various phylogenetic groups to the utilization of dissolved organic matter (DOM) depend solely on their relative abundance in the bacterial community. We found that utilization of even simple low-molecular-weight DOM components by bacteria differed across the major phylogenetic groups and often did not correlate with the relative abundance of these bacterial groups in estuarine and coastal environments. The CytophagaFlavobacter cluster was overrepresented in the portion of the assemblage consuming chitin, N-acetylglucosamine, and protein but was generally underrepresented in the assemblage consuming amino acids. The amino acid-consuming assemblage was usually dominated by the ␣ subclass of the class Proteobacteria, although the representation of ␣-proteobacteria in the protein-consuming assemblages was about that expected from their relative abundance in the entire bacterial community. In our experiments, no phylogenetic group dominated the consumption of all DOM, suggesting that the participation of a diverse assemblage of bacteria is essential for the complete degradation of complex DOM in the oceans. These results also suggest that the role of aerobic heterotrophic bacteria in carbon cycling would be more accurately described by using three groups instead of the single bacterial compartment currently used in biogeochemical models.Analysis of 16S rRNA gene sequences (15) has greatly advanced our understanding of the phylogenetic diversity of bacteria and archaea (18), especially that of the vast majority of microbes in nature that have resisted cultivation to date (2). There is little information, however, on the metabolic function of specific bacterial groups in natural assemblages since few culture-independent studies have linked bacterial community structure and function (6). Although information on phylogenetic relationships of uncultured bacteria is readily accessible (14), the inability to culture most microbes limits the opportunities to assess their metabolic diversity. Even if appropriate culture conditions were to be found for the bulk of marine microbes, bacterial metabolism in the sea would probably remain poorly described, since metabolic behavior in culture is likely different from that in situ.Extensive biogeochemical studies have shown that uptake and mineralization of dissolved organic matter (DOM) by bacteria constitute a major component of carbon cycling in aquatic ecosystems (11). Although the importance of DOM uptake is well recognized, the relative contributions of the major phylogenetic groups of bacteria to DOM uptake in the oceans are unknown (29). Differences in usage of various DOM components may help explain the distribution of the major bacterial groups among soil, freshwater, and marine ecosystems (18). It may also be important to know the minimum number of bacterial phylogen...

Hydrocarbon biodegradation by Arctic sea-ice and sub-ice microbial communities during microcosm experiments, Northwest Passage (Nunavut, Canada)

“…These changes agree with previous observations of a Bacteroidetes predominance associated with high bacterial biomass and production (Teira et al 2008). Bacteroidetes are the main degraders of complex polymeric organic compounds (Cottrell & Kirchman 2000;Fernández-Gómez et al 2013); therefore the presence of extracellular polymeric substances (EPS) in the sea ice of the Canadian Arctic Archipelago (Aslam et al 2016) could have provided a competitive advantage for resources to the Bacteroidetes over the Gammaproteobacteria. Conversely, the low organic matter content in sub-ice seawater (Table 1) could have been more advantageous for the Gammaproteobacteria.…”

Climate‐related changes of soil characteristics affect bacterial community composition and function of high altitude and latitude lakes

“…This agrees with previous observations from field (Crump et al ., 2003; Roiha et al ., 2011) and laboratory experiments (Logue et al ., 2016) showing that rapid shifts in community composition take place upon soil organic matter input. The loss and prevalence of the taxa determined in our study may be explained by their different functional adaptability, including differences in resource affinities (Cottrell & Kirchman, 2000; Salcher et al ., 2011; Heinrich et al ., 2013), physiological characteristics (Hahn & Pöckl, 2005; Šimek et al ., 2006) and genetic composition (Bauer et al ., 2006; Gómez‐Pereira et al ., 2012; Teeling et al ., 2012; Tveit et al ., 2013). Further, changes in lake bacterial community composition have been attributed not only to the differential response of individual bacterial taxa to DOM inputs, but also to the introduction of soil bacteria with allochthonous sources or to incubation effects (Crump et al ., 2003; Logue et al ., 2016).…”

“…In any case, it is evident that bacteria interact in a complex way, partly depending on competition for or facilitation of resource utilization (Fuhrman et al ., 2015). It can be assumed that the effects of soil source on bacterial community composition and succession were direct and mediated through a combination of ecological lifestyles (copiotrophs vs. oligotrophs) and taxon‐specific substrate preferences (specialists vs. generalists) (Cottrell & Kirchman, 2000; Eiler et al ., 2003; Salcher et al ., 2013; Pérez et al ., 2015), as well as through species interactions.…”

“…2011). In turn, bacterial communities have been shown to respond quickly to variation in substrate availability and concentration, often favouring opportunistic bacteria such as members of Betaproteobacteria (Burkert et al ., 2003; Šimek et al ., 2005; Hornák et al ., 2006; Posch et al ., 2007) or Bacteroidetes (Cottrell & Kirchman, 2000; Battin et al ., 2001; Eiler et al ., 2003; Zeder et al ., 2009). Besides the critical role of heterotrophic bacteria in processing soil‐derived organic matter in inland waters, knowledge on covarying factors, such as the release from nutrient limitation during pulses of soil run off in high altitude and latitude lakes remains limited (Pérez & Sommaruga, 2006).…”

Towards a better understanding of microbial carbon flux in the sea*

“…It is true that we do not fully understand the ecological consequences of the described bacterial (micro) diversity (Acinas et al 2004, Thompson et al 2005), but we have been able to show clear trends in the use of selected molecular weight size fractions and molecular types by large phylogenetic groups (e.g. Cottrell & Kirchman 2000, Alonso-Sáez & Gasol 2007, indicating that most bacteria within a specific cluster seem to behave similarly, at least on a general functional level. However, as revealed in a study testing the effect of photosynthetically active radiation (PAR) and ultraviolet (UV) radiation on different groups of marine bacteria, the phylogenetic level targeted by the oligonucleotide probe was decisive for the outcome of the experiment (see sections 'A specific example: bacteria on the dark side' and 'Role of aerobic anoxygenic phototrophs in the marine carbon cycle' below).…”