Altitudinal Patterns of Diversity and Functional Traits of Metabolically Active Microorganisms in Stream Biofilms

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Altitudinal Patterns of Diversity and Functional Traits of Metabolically Active Microorganisms in Stream Biofilms The ISME Journal (2015) 9, 2454–2464 © 2015 International Society for Microbial Ecology All rights reserved 1751-7362/15 www.nature.com/ismej ORIGINAL ARTICLE Altitudinal patterns of diversity and functional traits of metabolically active microorganisms in stream biofilms Linda Wilhelm1, Katharina Besemer2, Lena Fragner3, Hannes Peter4, Wolfram Weckwerth3 and Tom J Battin1,5 1Department of Limnology and Oceanography, Faculty of Life Sciences, University of Vienna, Vienna, Austria; 2School of Engineering, University of Glasgow, Glasgow, UK; 3Department of Ecogenomics and Systems Biology, University of Vienna, Vienna, Austria; 4Lake and Glacier Ecology Research Group, Institute of Ecology, University of Innsbruck, Innsbruck, Austria and 5Stream Biofilm and Ecosystem Research Laboratory, School of Architecture, Civil and Environmental Engineering, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland Resources structure ecological communities and potentially link biodiversity to energy flow. It is commonly believed that functional traits (generalists versus specialists) involved in the exploitation of resources depend on resource availability and environmental fluctuations. The longitudinal nature of stream ecosystems provides changing resources to stream biota with yet unknown effects on microbial functional traits and community structure. We investigated the impact of autochthonous (algal extract) and allochthonous (spruce extract) resources, as they change along alpine streams from above to below the treeline, on microbial diversity, community composition and functions of benthic biofilms. Combining bromodeoxyuridine labelling and 454 pyrosequencing, we showed that diversity was lower upstream than downstream of the treeline and that community composition changed along the altitudinal gradient. We also found that, especially for allochthonous resources, specialisation by biofilm bacteria increased along that same gradient. Our results suggest that in streams below the treeline biofilm diversity, specialisation and functioning are associated with increasing niche differentiation as potentially modulated by divers allochthonous and autochthonous constituents contributing to resources. These findings expand our current understanding on biofilm structure and function in alpine streams. The ISME Journal (2015) 9, 2454–2464; doi:10.1038/ismej.2015.56; published online 15 May 2015 Introduction characterise DOC in streams above the treeline, whereas terrestrial deliveries increasingly add to In headwater streams, the smallest and most abun- the carbon pool further downstream (Battin et al., dant in stream networks, dissolved organic carbon 2004; Milner et al., 2009; Zah and Uehlinger, 2001). (DOC) constitutes the primary resource for microbial Several studies have reported DOC source and heterotrophs. DOC encompasses a large pool composition as potential drivers of microbial com- of molecules, which depending on their source munity structure and functioning in streams (e.g., (i.e., autochthonous versus allochthonous), can Kaplan and Bott, 1989; Sun et al., 1997; Peter et al., vary in chemical composition and bioavailability 2011) and in lakes (e.g., Crump et al., 2003; Judd (e.g., Sun et al., 1997; Jaffé et al., 2012). Allochtho- et al., 2006). However, only few have studied the nous constituents typically dominate the DOC pool, relationship between DOC characteristics and micro- with the exception of alpine and arid catchments bial functional traits in streams (McArthur et al., devoid of major terrestrial vegetation (e.g., Milner 1985; Koetsier et al., 1997). Although with a et al., 2009). In alpine streams, autochthonous traditional focus on plants and animals, the concept deliveries from algal production (and mosses) of functional traits (i.e., specialists versus general- ists) now becomes increasingly established in micro- Correspondence: TJ Battin, Stream Biofilm and Ecosystem bial ecology with notable examples from soil Research Laboratory, School of Architecture, Civil and Environ- (Lennon et al., 2012), wastewater (Muller et al., mental Engineering, École Polytechnique Fédérale de Lausanne, 2014) and marine ecosystems (Mou et al., 2008). Lausanne 1015, Switzerland. E-mail: [email protected] Understanding the relationship between microbial Received 26 November 2014; revised 4 February 2015; accepted community structure and specialisation in response 9 March 2015; published online 15 May 2015 to resources may shed new light on the ecological Stream biofilm diversity and functional traits L Wilhelm et al 2455 mechanisms underlying the carbon cycling in stream hand, were expected to support microbial specialists ecosystems (Battin et al., 2008). However, trait for both autochthonous and allochthonous DOC distribution and the role of functional redundancy constituents. As resource diversity increases down- remain elusive in stream biofilms, especially when stream, resource partitioning among microbial taxa multiple functions are considered simultaneously may increase, allowing for lower multifunctional (Gamfeldt et al., 2008; Hillebrand and Matthiessen, redundancy in streams below the treeline. 2009). The high diversity of microbial communities The stochastic nature of hydrology and sedimen- makes the characterisation of functional traits and tary dynamics in streams creates pronounced hetero- the investigation of functional redundancy challen- geneity in resource availability and biodiversity ging. To circumvent this bottleneck, we exposed patterns (Townsend, 1989). It is assumed that these microorganisms to the thymidine analogue bromo- environmental fluctuations relieve invertebrate deoxyuridine (BrdU) and sequenced the BrdU- species from competition, which would favour labelled DNA after immunocapturing (Yin et al., generalists rather than specialists (Townsend, 1989; 2000); this allowed us to identify metabolically Schoener, 1974; Rosenfeld, 2002). At the same time, active microorganisms upon amendment with model it is established that resource partitioning allows autochthonous and allochthonous DOC, respectively invertebrates to assemble diverse communities along (Mou et al., 2008). Extracts were amended to benthic the stream continuum. The relationships between biofilms grown in situ above, around and below the downstream shifts in resources (i.e., primarily treeline in three alpine catchments, allowing us to autochthonous sources upstream versus more study diversity patterns of metabolically active allochthonous sources downstream), hydro- biofilm communities and to relate these patterns to geomorphology and biotic communities have been resource specialisation. described by the River Continuum Concept (Vannote et al., 1980). Microorganisms were not encapsulated in the River Continuum Concept, and yet evidence Materials and methods increasingly suggests that microbial communities predictably change along the river continuum Study sites and biofilm growth (Besemer et al., 2013; Read et al., 2014; Savio Our study sites included three headwater streams et al., 2014). However, the potential drivers of these (Obertalbach = OTB, Steinriesenbach = SRB, Riesach- patterns remain poorly understood, which is bach = RB) in the Schladminger Tauern, Austria, noticeable, given the relevance of microorganisms ranging from 1114 to 2275 m above sea level (a.s.l.). for stream ecosystem functions (Battin et al., 2008). Sparse alpine grassland and meadow dominate The aim of this study was to investigate microbial vegetation above the treeline (around 1600 m a.s.l), community structure, diversity and functional traits whereas spruce (Picea abies) dominates vegetation (generalists versus specialists) and redundancy in below the treeline. Streamwater chemistry was benthic biofilms of Alpine streams in response to comparable across all three catchments with resources that potentially change from upstream very low electrical conductivity (average ± s.d.: − 1 to downstream of the treeline. We hypothesised that 33.3 ± 17.7 μScm ) and reduced pH (7.1 ± 0.5) typi- microbial community structure and diversity change cal of the crystalline geology (gneissic rock) along such altitudinal gradients and that resource (Supplementary Table 1). DOC concentration was − 1 specialisation contributes to these patterns. Mixing generally low (0.48 ± 0.19 mg C l ) and tended to of resources from various sources along the long- increase in SRB and RB, but less in OTB. Nitrate μ − 1 itudinal continuum of streams may increase sub- (189.9 ± 91.4 g N-NO3 l ) clearly increased down- strate diversity and reduce its relative dominance by stream in all catchments. We grew benthic biofilms averaging. Although microbial generalists may be on initially sterile unglazed ceramic tiles (surface 2 able to better cope with pronounced environmental area: 2 cm ) for 8 weeks in all stream reaches in June and resource fluctuations upstream of the treeline, (2011); tiles were shaded to prevent copious algal we expect that microbial specialists increasingly growth. Biofilms were grown across an altitudinal establish downstream because of potentially increas- (and longitudinal) gradient above, around and below ing resource diversity. Hence, we postulated that the the treeline (Supplementary Table 1 for altitudes). relative importance of microbial specialists versus Biofilm samples were transported within 3 h in μ generalists would increase downstream of the tree- sterile containers filled with 0.2 m-filtered stream- line where both autochthonous and allochthonous water (cooled,
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