Temporal variability and coherence of euphotic zone bacterial communities over a decade in the Southern California Bight

The ISME Journal (2013) 7, 2259–2273 & 2013 International Society for Microbial Ecology All rights reserved 1751-7362/13 www.nature.com/ismej ORIGINAL ARTICLE Temporal variability and coherence of euphotic zone bacterial communities over a decade in the Southern California Bight Cheryl-Emiliane T Chow, Rohan Sachdeva, Jacob A Cram, Joshua A Steele, David M Needham, Anand Patel, Alma E Parada and Jed A Fuhrman Department of Biological Sciences, University of Southern California, Los Angeles, CA, USA Time-series are critical to understanding long-term natural variability in the oceans. Bacterial communities in the euphotic zone were investigated for over a decade at the San Pedro Ocean Time-series station (SPOT) off southern California. Community composition was assessed by Automated Ribosomal Intergenic Spacer Analysis (ARISA) and coupled with measurements of oceanographic parameters for the surface ocean (0–5 m) and deep chlorophyll maximum (DCM, average depth B30 m). SAR11 and cyanobacterial ecotypes comprised typically more than one-third of the measured community; diversity within both was temporally variable, although a few operational taxonomic units (OTUs) were consistently more abundant. Persistent OTUs, mostly Alphaproteobacteria (SAR11 clade), Actinobacteria and Flavobacteria, tended to be abundant, in contrast to many rarer yet intermittent and ephemeral OTUs. Association networks revealed potential niches for key OTUs from SAR11, cyanobacteria, SAR86 and other common clades on the basis of robust correlations. Resilience was evident by the average communities drifting only slightly as years passed. Average Bray-Curtis similarity between any pair of dates was B40%, with a slight decrease over the decade and obvious near-surface seasonality; communities 8–10 years apart were slightly more different than those 1–4 years apart with the highest rate of change at 0–5 m between communities o4 years apart. The surface exhibited more pronounced seasonality than the DCM. Inter-depth Bray-Curtis similarities repeatedly decreased as the water column stratified each summer. Environmental factors were better predictors of shifts in community composition than months or elapsed time alone; yet, the best predictor was community composition at the other depth (that is, 0–5 m versus DCM). The ISME Journal (2013) 7, 2259–2273; doi:10.1038/ismej.2013.122; published online 18 July 2013 Subject Category: Microbial population and community ecology Keywords: marine bacterioplankton; ARISA; community ecology; microbe–microbe interactions; time series Introduction Investigations into temporal dynamics of marine microbial communities have revealed remarkable similarities and dissimilarities between ocean basins and have provided insight into the complex ecology of microbes (as reviewed in Ducklow et al. (2009); Fuhrman (2009); Giovannoni and Vergin (2012)). A holistic understanding of microbes in the ocean requires knowledge of the following: which microbes are present, when they occur, how much they contribute to the community and what environmental factors facilitate their distribution. Correspondence: C-ET Chow, Department of Earth, Ocean, and Atmospheric Sciences, University of British Columbia, 2020 - 2207 Main Mall, Vancouver, British Columbia, Canada V6T 1Z4. E-mail: Received 22 October 2012; revised 12 June 2013; accepted 18 June 2013; published online 18 July 2013 Knowledge of each parameter will improve models of the microbial loop and microbial roles in the sea. Seasonal and monthly patterns of variation have been observed using molecular methods at multiple aquatic time-series sites, which suggest that environmental change elicits a biological response; many, but not all, have also shown recurrence (Acinas et al., 1997; Li, 1998; Morris et al., 2005; Fuhrman et al., 2006; Alonso Sáez et al., 2007; Kan et al., 2007; Treusch et al., 2009; Campbell et al., 2011; Eiler et al., 2011; Gilbert et al., 2012; Robidart et al., 2012). For example, seasonality in Synechococcus ecotypes was observed in the Southern California Bight, primarily for clades I and IV (Tai and Palenik, 2009), and in the Chesapeake Bay (Cai et al., 2010). Distribution of Prochlorococcus ecotypes at the Hawaii Ocean Time-series (HOT) and Bermuda Atlantic Time-series Study (BATS) was similar except during annual deep water column mixing events at BATS (Morris et al., 2005; Treusch et al., Bacterial variability over a decade at SPOT C-ET Chow et al 2260 2009; Malmstrom et al., 2010; Eiler et al., 2011). SAR11 ecotypes were also dominant yet variable over time at BATS and HOT (Morris et al., 2002; Carlson et al., 2009; Eiler et al., 2009; Giovannoni and Vergin, 2012). Seasonal patterns were also seen using next-generation sequencing (for example, Andersson et al., 2010; Fortunato et al., 2012; Gilbert et al., 2012). In this study, we examined bacterial community structure in light of traditional ecological metrics for community composition, membership, phylogeny, persistence and connectivity (recently reviewed in Shade and Handelsman (2012)). Prior research at the San Pedro Ocean Time-series (SPOT) has focused on determining the temporal variability of bacterial, archaeal and protistan taxa and the development of ecological networks that link these communities (Countway and Caron, 2006; Fuhrman et al., 2006; Beman et al., 2010; Countway et al., 2010; Beman et al., 2011; Steele et al., 2011). Here, we assessed inter-annual, seasonal and monthly variability and resilience of bacterial communities in the surface water and deep chlorophyll maximum (DCM), as revealed by Automated Ribosomal Intergenic Spacer Analysis (ARISA), over a full decade. ARISA allowed for repeated detection of the same microbes over time and their relative abundance within the bacterial community; OTUs (operational taxonomic units) were identified by their unique fragment lengths, and each was assigned an identity through the coupling of 16S-ITS sequences from SPOT and elsewhere to an observed (or predicted) ARISA fragment length. We discuss the roles of specific bacterial taxa using correlated partners from network analysis and as members of a newly defined core microbiome at SPOT, as well as the diversity within key bacterial groups, and temporal patterns in relative abundances of taxonomically related OTUs. We also determine which of the measured environmental parameters best explain the observed community structure. Materials and methods Sample Collection Seawater was collected approximately monthly from August 2000 to January 2011 at 0–5 m and the DCM (average 28.2 m, range 7–45 m), as determined from in situ fluorescence, at SPOT (331330 N, 1181240 W). After losses due to weather conditions or due to equipment failure, 103 months were sampled at 0–5 m and 89 months at DCM over 126 months. DNA was extracted by phenol-chloroform from B10 l of seawater serially filtered through a 142 mm Type A/E glass-fiber filter (Pall Life Sci (...truncated)