Microbial community structure and function on sinking particles in the North Pacific Subtropical Gyre

Kristina M Fontanez,David M Karl,Ty J Samo,John M Eppley,Edward F Delong

doi:10.3389/fmicb.2015.00469

Abstract

Sinking particles mediate the transport of carbon and energy to the deep-sea, yet the specific microbes associated with sedimenting particles in the ocean's interior remain largely uncharacterized. In this study, we used particle interceptor traps (PITs) to assess the nature of particle-associated microbial communities collected at a variety of depths in the North Pacific Subtropical Gyre. Comparative metagenomics was used to assess differences in microbial taxa and functional gene repertoires in PITs containing a preservative (poisoned traps) compared to preservative-free traps where growth was allowed to continue in situ (live traps). Live trap microbial communities shared taxonomic and functional similarities with bacteria previously reported to be enriched in dissolved organic matter (DOM) microcosms (e.g., Alteromonas and Methylophaga), in addition to other particle and eukaryote-associated bacteria (e.g., Flavobacteriales and Pseudoalteromonas). Poisoned trap microbial assemblages were enriched in Vibrio and Campylobacterales likely associated with eukaryotic surfaces and intestinal tracts as symbionts, pathogens, or saprophytes. The functional gene content of microbial assemblages in poisoned traps included a variety of genes involved in virulence, anaerobic metabolism, attachment to chitinaceaous surfaces, and chitin degradation. The presence of chitinaceaous surfaces was also accompanied by the co-existence of bacteria which encoded the capacity to attach to, transport and metabolize chitin and its derivatives. Distinctly different microbial assemblages predominated in live traps, which were largely represented by copiotrophs and eukaryote-associated bacterial communities. Predominant sediment trap-assocaited eukaryotic phyla included Dinoflagellata, Metazoa (mostly copepods), Protalveolata, Retaria, and Stramenopiles. These data indicate the central role of eukaryotic taxa in structuring sinking particle microbial assemblages, as well as the rapid responses of indigenous microbial species in the degradation of marine particulate organic matter (POM) in situ in the ocean's interior.

Highlights

Particulate organic matter (POM) generated in the euphotic zone is the major conduit of matter and energy transport to the deep sea and represents the primary mechanism of carbon removal from surface waters via the biological pump (McCave, 1975; Volk and Hoffert, 1985)
Sinking particles represent the primary vehicles of organic carbon flux from surface waters to the deep ocean (Volk and Hoffert, 1985), yet to date, few data are available on the specific microbes and metabolic pathways responsible for POM degradation throughout the water column
Sediment trap metagenomic analyses revealed dramatic differences in the taxonomic diversity and functional potential of microbes associated with sinking particles in poisoned sediment traps, compared to those that grew in situ in live traps

Summary

Introduction

Particulate organic matter (POM) generated in the euphotic zone is the major conduit of matter and energy transport to the deep sea and represents the primary mechanism of carbon removal from surface waters via the biological pump (McCave, 1975; Volk and Hoffert, 1985). Analysis of whole seawater segregated into particle-associated (>1 μm) and free-living size fractions has revealed taxonomically and functionally distinct microbial communities in marine anoxic zones (Ganesh et al, 2014), coastal ecosystems (Allen et al, 2012; Smith et al, 2013), estuarine environments (Crump et al, 1999; Waidner and Kirchman, 2007), inland seas (Moeseneder et al, 2001; Fuchsman et al, 2011, 2012; Crespo et al, 2013), phytoplankton blooms (Riemann et al, 2000; Fandino et al, 2005; Teeling et al, 2012), ocean trenches (Eloe et al, 2011), and the open ocean (Kellogg and Deming, 2009; Allen et al, 2012) These studies have shown that in particular, members of the Bacteroidetes, Planctomycetes, and Deltaproteobacteria are often enriched in larger particle size fractions. While sediment traps have proven useful for over 30 years in studies of sinking POM (Karl and Knauer, 1984), to date there exists only one report of the phylogenetic diversity of sedimenttrap collected microbes, which grew over 24 h in sediment-trap captured particles from 100 to 120 m (LeCleir et al, 2013)

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Conclusion