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Microbial Communities Network Structure Across Strong Environmental Gradients: How Do bioRxiv preprint doi: https://doi.org/10.1101/2021.06.08.445284; this version posted June 9, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Microbial communities network structure across strong environmental gradients: How do 2 they compare to macroorganisms? 3 Arboleda-Baenaa,b, C.M; Freilichc,d, M. A; Pareja, C.Bb; Logares, Re; De la Iglesia, Rb,f; 4 Navarrete, S.A a,f 5 a Estación Costera de Investigaciones Marinas, Center for Applied Ecology and Sustainability 6 (CAPES), Millenium Nucleus NUTME, Pontificia Universidad Católica de Chile, Chile 7 b Laboratorio de Microbiología Marina, Departamento de Genética Molecular y Microbiología, 8 Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, Chile 9 c Department of Earth, Atmospheric and Planetary Science, Massachusetts Institute of 10 Technology, Cambridge, Massachusetts 02139 USA 11 d Department of Physical Oceanography, Woods Hole Oceanographic Institution,Woods Hole, 12 Massachusetts 02543 USA 13 e Instituto de Ciencias del Mar – CSIC, Paseo Marítimo de la Barceloneta, 37 – 49, 080003 14 Barcelona, Spain 15 f Marine Energy Research & Innovation Center (MERIC), Avda. Apoquindo 2827, Santiago, 16 Chile. 17 Corresponding author e-mail: [email protected] 18 1. Some data are already published, with those publications properly cited in this submission: 19 Broitman et al. 2001 and Freilich et al. 2018. 20 2. Sequence data will be deposited at the European Nucleotide Archive (ENA) public database 21 under accession number PRJEB45042 and released after the journal acceptance. 22 3. We don´t have novel code. But we will provide a copy in Github of the script used 23 (https://github.com/ClarArboledaBaena) after the journal acceptance with the Zenodo DOI. 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.08.445284; this version posted June 9, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 24 Abstract 25 The way strong environmental gradients shape multispecific assemblages has allowed us to 26 examine a suite of ecological and evolutionary hypotheses about structure, regulation, and 27 community responses to fluctuating environments. But whether the highly diverse co-occurring, 28 free-living microorganisms are shaped in similar ways as macroscopic organisms, across the 29 same gradients, has yet to be addressed in most ecosystems. The ‘everything is everywhere’ 30 hypothesis suggests they are not, at least not to the same extent. Here we characterize the 31 structure of intertidal microbial biofilm communities and compare the intensity of zonation at the 32 ‘species’ level, changes in taxonomic diversity and composition at the community level, and 33 network attributes, with those observed in co-occurring macroalgae and invertebrates. At the 34 level of species and OTUs, for dominant macro and microorganisms respectively, microbes 35 showed less variability across the tidal gradient than macroorganisms. At the community-level, 36 however, microbes and macro-organisms showed similarly strong patterns of tidal zonation, with 37 major changes in composition and relative abundances across tides. Moreover, the proportion of 38 ‘environmental specialists’ in different tidal zones was remarkably similar in micro and 39 macroscopic communities, and taxonomic richness and diversity followed similar trends, with 40 lower values in the high intertidal zone. Network analyses showed similar connectivity and 41 transitivity, despite the large differences in absolute richness between the groups. A high 42 proportion of positive co-occurrences within all tidal zones and mostly negative links between 43 the high and low tidal zones were observed among habitat specialist taxa of micro-and macro- 44 organisms. Thus, our results provide partial support to the idea that microbes are less affected by 45 environmental variability than macroscopic counterparts. At the species-level, the most common 46 microbe species exhibit less variation across tides than most common macroscopic organisms, 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.08.445284; this version posted June 9, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 47 suggesting the former perceive a more homogeneous environment and/or are more resistant to 48 the associated stress. At the community-level, most indicators of community and network 49 structure across the gradient are similar between microbes and macro-organisms, suggesting that 50 despite orders of magnitude differences in richness and size, these two systems respond to stress 51 gradients, giving rise to zonation patterns. 52 Key words: Zonation, microorganisms, co-occurrence networks, stress gradients, individual- 53 and community-responses, network attributes. 54 55 Introduction 56 Understanding the mechanisms and processes responsible for patterns of abundance and 57 distribution of species across environmental gradients is one of the main goals of community 58 ecology (Mittelbach and McGill 2019), and one of the most striking patterns is the zonation of 59 dominant organisms that occupy different parts of the environmental gradient. These patterns 60 have served as the basis to test core hypotheses about the organization of communities (e.g. 61 Whittaker 1959) and the ecological processes shaping fundamental and realized species’ niches, 62 such as physiological tolerances and species interactions (Connell 1961a, 1961b, Menge and 63 Sutherland 1987). However, this deep understanding of communities of macroscopic organisms 64 contrasts sharply with the still scarce knowledge about communities of free-living 65 microorganisms (Fontaneto 2011, Hanson et al. 2012). The ‘everything is everywhere, but the 66 environment selects’ hypothesis, set forth by Gerhard Baas Becking in the early 1930s, has 67 inspired much of the microbial biogeographical and ecological research of the past decades (de 68 Wit and Bouvier 2006, O’Malley 2007) and suggests that microbial communities are primarily 69 determined by moderate rates of dispersal and secondarily by environmental variation 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.08.445284; this version posted June 9, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 70 (selection). It is clear that microbial biodiversity is shaped by environmental gradients, especially 71 by those factors that alter soil or water pH (Rousk et al. 2010, Krause et al. 2012), temperature 72 (Logares et al. 2020), and resource availability (Follows et al. 2007). The local environment 73 ´selects´ which microorganisms are present and, like in macroscopic organisms, patterns of 74 abundance and composition across environmental gradients result from the constraints set by 75 abiotic conditions and the interactions among co-occurring microbes (Fontaneto 2011, Hanson et 76 al. 2012, Mandakovic et al. 2018). Yet, the question remains, are communities of microbial 77 organisms less structured across the same environmental gradients than their co-occurring 78 macroscopic counterparts? If both vary across sharp environmental gradients, are the patterns of 79 community structure towards the stressful and benign ends of a gradient similar to those 80 observed in macroscopic organisms? Addressing these and other similar questions allows us to 81 challenge our ecological models and get valuable insight into how different is the organization 82 between the micro and macroscopic worlds. 83 Probably the most studied zonation pattern is the one occurring between the highest and lowest 84 tides along most marine rocky shores of the world (Barnes and Hughes 1999, Raffaelli and 85 Hawkins 2012). In this habitat, environmental conditions range from entirely aquatic to 86 completely terrestrial in a few meters (Thompson et al. 2002, Harley and Helmuth 2003); and, 87 within their absolute tolerance limits, species become consistently more abundant at some tidal 88 levels than others (Stephenson and Stephenson 1949, Connell 1961a, 1961b). Also, co- 89 occurrence network analyses show modules (cluster of species highly connected) related to a 90 specific zonation band due mainly driven by shared environmental preferences (Freilich et al. 91 2018). Beyond the tidal regime that sets the stage for the stress gradient (Denny and Paine 1998, 92 Raffaelli and Hawkins 2012), intertidal zonation of macroscopic organisms results from multiple 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.08.445284; this version posted June 9, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 93 interactive physical factors, including wave exposure and the
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