Jürg Brendan Logue

Empirical approaches to metacommunities: a review and comparison with theory

Metacommunity theory has advanced understanding of how spatial dynamics and local interactions shape community structure and biodiversity. Here, we review empirical approaches to metacommunities, both observational and experimental, pertaining to how well they relate to and test theoretical metacommunity paradigms and how well they capture the realities of natural ecosystems. First, we show that the species-sorting and mass-effects paradigms are the most commonly tested and supported paradigms. Second, the dynamics observed can often be ascribed to two or more of the four non-exclusive paradigms. Third, empirical approaches relate only weakly to the concise assumptions and predictions made by the paradigms. Consequently, we suggest major avenues of improvement for empirical metacommunity approaches, including the integration across theoretical approaches and the incorporation of evolutionary and meta-ecosystem dynamics. We hope for metacommunity ecology to thereby bridge existing gaps between empirical and theoretical work, thus becoming a more powerful framework to understand dynamics across ecosystems.

Unraveling assembly of stream biofilm communities.

Microbial biofilms assemble from cells that attach to a surface, where they develop into matrix-enclosed communities. Mechanistic insights into community assembly are crucial to better understand the functioning of natural biofilms, which drive key ecosystem processes in numerous aquatic habitats. We studied the role of the suspended microbial community as the source of the biofilm community in three streams using terminal-restriction fragment length polymorphism and 454 pyrosequencing of the 16S ribosomal RNA (rRNA) and the 16S rRNA gene (as a measure for the active and the bulk community, respectively). Diversity was consistently lower in the biofilm communities than in the suspended stream water communities. We propose that the higher diversity in the suspended communities is supported by continuous inflow from various sources within the catchment. Community composition clearly differed between biofilms and suspended communities, whereas biofilm communities were similar in all three streams. This suggests that biofilm assembly did not simply reflect differences in the source communities, but that certain microbial groups from the source community proliferate in the biofilm. We compared the biofilm communities with random samples of the respective community suspended in the stream water. This analysis confirmed that stochastic dispersal from the source community was unlikely to shape the observed community composition of the biofilms, in support of species sorting as a major biofilm assembly mechanism. Bulk and active populations generated comparable patterns of community composition in the biofilms and the suspended communities, which suggests similar assembly controls on these populations.

Biogeography of bacterial communities exposed to progressive long-term environmental change

The response of microbial communities to long-term environmental change is poorly understood. Here, we study bacterioplankton communities in a unique system of coastal Antarctic lakes that were exposed to progressive long-term environmental change, using 454 pyrosequencing of the 16S rDNA gene (V3–V4 regions). At the time of formation, most of the studied lakes harbored marine-coastal microbial communities, as they were connected to the sea. During the past 20 000 years, most lakes isolated from the sea, and subsequently they experienced a gradual, but strong, salinity change that eventually developed into a gradient ranging from freshwater (salinity 0) to hypersaline (salinity 100). Our results indicated that present bacterioplankton community composition was strongly correlated with salinity and weakly correlated with geographical distance between lakes. A few abundant taxa were shared between some lakes and coastal marine communities. Nevertheless, lakes contained a large number of taxa that were not detected in the adjacent sea. Abundant and rare taxa within saline communities presented similar biogeography, suggesting that these groups have comparable environmental sensitivity. Habitat specialists and generalists were detected among abundant and rare taxa, with specialists being relatively more abundant at the extremes of the salinity gradient. Altogether, progressive long-term salinity change appears to have promoted the diversification of bacterioplankton communities by modifying the composition of ancestral communities and by allowing the establishment of new taxa.

Regional invariance among microbial communities

Microbial ecology has focused much on causes of between-site variation in community composition. By analysing five data-sets each of aquatic bacteria and phytoplankton, we demonstrated that microbial communities show a large degree of similarity in community composition and that abundant taxa were widespread, a typical pattern for many metazoan metacommunities. The regional abundance of taxa explained on average 85 and 41% of variation in detection frequency and 58 and 31% of variation in local abundances for bacteria and phytoplankton, respectively. However, regional abundance explained less variation in local abundances with increasing environmental variation between sites within data-sets. These findings indicate that the studies of microbial assemblages need to consider similarities between communities to better understand the processes underlying the assembly of microbial communities. Finally, we propose that the degree of regional invariance can be linked to the evolution of microbes and the variation in ecosystem functions performed by microbial communities.

Which sequencing depth is sufficient to describe patterns in bacterial α- and β-diversity?

The vastness of microbial diversity implies that an almost infinite number of individuals needs to be identified to accurately describe such communities. Practical and economical constraints may therefore prevent appropriate study designs. However, for many questions in ecology it is not essential to know the actual diversity but rather the trends among samples thereof. It is, hence, important to know to what depth microbial communities need to be sampled to accurately measure trends in diversity. We used three data sets of freshwater and sediment bacteria, where diversity was explored using 454 pyrosequencing. Each data set contained 6-15 communities from which 15 000-20 000 16S rRNA gene sequences each were obtained. These data sets were subsampled repeatedly to 10 different depths down to 200 sequences per community. Diversity estimates varied with sequencing depth, yet, trends in diversity among samples were less sensitive. We found that 1000 denoised sequences per sample explained to 90% the trends in β-diversity (Bray-Curtis index) among samples observed for 15 000-20 000 sequences. Similarly, 5000 denoised sequences were sufficient to describe trends in α-diversity (Shannon index) with the same accuracy. Further, 5000 denoised sequences captured to more than 80% the trends in Chao1 richness and Pielous evenness.

Species sorting affects bacterioplankton community composition as determined by 16S rDNA and 16S rRNA fingerprints

To understand the mechanisms determining community composition, it is essential to distinctively unravel the importance of local from that of regional processes. In this effort, the mechanisms underlying bacterioplankton community assembly were analysed in eight lakes of short water residence time (WRT) during a four-season sampling campaign. Bacterioplankton community composition (BCC) was determined using terminal-restriction fragment length polymorphism (t-RFLP) on the 16S rRNA gene (16S rDNA) and 16S rRNA. The relationship between similarity in BCC between a lake and its major inlet on the one hand and cell import per cell production rate from the inlet to the lake epilimnion on the other was used as a measure of the importance of cell dispersal (mass effects) for community assembly. Low similarities in BCC between lakes and their inlets were observed even at short WRTs, and the degree of similarity correlated better with the environmental conditions in lakes and streams than with cell import per cell production rates. Thus, mass effects seemed less important for local lake BCC in comparison to environmental habitat characteristics (species sorting). Analyses of 16S rDNA and 16S rRNA community fingerprints yielded similar results, indicating that species-sorting dynamics exerted an equally important effect on both the abundant and active fraction within the studied bacterioplankton communities.

Biogeography of bacterioplankton in inland waters.

Abstract Bacteria are among the most abundant groups of organisms. They mediate key ecological processes. Recent molecular advances have provided greater insight into bacterial diversity as well as allowing a more thorough examination of patterns in the spatial and temporal distribution of bacteria. Thus, the study of bacterial biodiversity and biogeographical distribution has stimulated considerable interest and dispute over the last decade. This review summarises the findings obtained from studies on the biogeography of bacterioplankton in inland waters. We examine factors and processes that may determine and maintain bacterial diversity and biogeography, and relate these to the theoretical metacommunity framework. We conclude that the importance of local environmental factors (such as lake character) for local bacterioplankton community compositions (BCC) is much more intensively studied than the importance of regional factors, such as dispersal. Further, few attempts have been made to evaluate simultaneously the relative importance of the two types of factors for BCC. Finally, we summarise gaps in knowledge, delineate challenges and put forward possible future research directions.

Experimental insights into the importance of aquatic bacterial community composition to the degradation of dissolved organic matter.

Bacteria play a central role in the cycling of carbon, yet our understanding of the relationship between the taxonomic composition and the degradation of dissolved organic matter (DOM) is still poor. In this experimental study, we were able to demonstrate a direct link between community composition and ecosystem functioning in that differently structured aquatic bacterial communities differed in their degradation of terrestrially derived DOM. Although the same amount of carbon was processed, both the temporal pattern of degradation and the compounds degraded differed among communities. We, moreover, uncovered that low-molecular-weight carbon was available to all communities for utilisation, whereas the ability to degrade carbon of greater molecular weight was a trait less widely distributed. Finally, whereas the degradation of either low- or high-molecular-weight carbon was not restricted to a single phylogenetic clade, our results illustrate that bacterial taxa of similar phylogenetic classification differed substantially in their association with the degradation of DOM compounds. Applying techniques that capture the diversity and complexity of both bacterial communities and DOM, our study provides new insight into how the structure of bacterial communities may affect processes of biogeochemical significance.

Freshwater bacterioplankton richness in oligotrophic lakes depends on nutrient availability rather than on species-area relationships

A central goal in ecology is to grasp the mechanisms that underlie and maintain biodiversity and patterns in its spatial distribution can provide clues about those mechanisms. Here, we investigated what might determine the bacterioplankton richness (BR) in lakes by means of 454 pyrosequencing of the 16S rRNA gene. We further provide a BR estimate based upon a sampling depth and accuracy, which, to our knowledge, are unsurpassed for freshwater bacterioplankton communities. Our examination of 22 669 sequences per lake showed that freshwater BR in fourteen nutrient-poor lakes was positively influenced by nutrient availability. Our study is, thus, consistent with the finding that the supply of available nutrients is a major driver of species richness; a pattern that may well be universally valid to the world of both micro- and macro-organisms. We, furthermore, observed that BR increased with elevated landscape position, most likely as a consequence of differences in nutrient availability. Finally, BR decreased with increasing lake and catchment area that is negative species–area relationships (SARs) were recorded; a finding that re-opens the debate about whether positive SARs can indeed be found in the microbial world and whether positive SARs can in fact be pronounced as one of the few ‘laws’ in ecology.

Editorial: Microbial Responses to Environmental Changes

Earth is teeming with taxonomically, phylogenetically, and metabolically highly diverse micro-organisms; organisms that are crucial for sustaining life on our planet in that they carry out processes of great biogeochemical significance. The processes and mechanisms underlying their diversity and distribution are, thus, of great interest, yet—despite their importance—only poorly understood.