Differing Growth Responses of Major Phylogenetic Groups of Marine Bacteria to Natural Phytoplankton Blooms in the Western North Pacific Ocean

Abstract

Growth and productivity of phytoplankton substantially change organic matter characteristics, which affect bacterial abundance, productivity, and community structure in aquatic ecosystems. We analyzed bacterial community structures and measured activities inside and outside phytoplankton blooms in the western North Pacific Ocean by using bromodeoxyuridine immunocytochemistry and fluorescence in situ hybridization (BIC-FISH). Roseobacter/Rhodobacter, SAR11, Betaproteobacteria, Alteromonas, SAR86, and Bacteroidetes responded differently to changes in organic matter supply. Roseobacter/Rhodobacter bacteria remained widespread, active, and proliferating despite large fluctuations in organic matter and chlorophyll a (Chl-a) concentrations. The relative contribution of Bacteroidetes to total bacterial production was consistently high. Furthermore, we documented the unexpectedly large contribution of Alteromonas to total bacterial production in the bloom. Bacterial abundance, productivity, and growth potential (the proportion of growing cells in a population) were significantly correlated with Chl-a and particulate organic carbon concentrations. Canonical correspondence analysis showed that organic matter supply was critical for determining bacterial community structures. The growth potential of each bacterial group as a function of Chl-a concentration showed a bell-shaped distribution, indicating an optimal organic matter concentration to promote growth. The growth of Alteromonas and Betaproteobacteria was especially strongly correlated with organic matter supply. These data elucidate the distinctive ecological role of major bacterial taxa in organic matter cycling during open ocean phytoplankton blooms.The major ecological function of heterotrophic bacteria in interactions with phytoplankton is mineralization of organic matter for recycling of nutrients and secondary production, which is channeled mainly to the higher trophic levels of aquatic food webs (10, 66). Growth of phytoplankton leads to major changes in organic matter quantity and quality, which results in changes to bacterial community structure, abundance, and productivity (3). Previous studies have shown that bacterial abundance, production, and community structure change markedly during naturally occurring and experimentally induced phytoplankton blooms (16,56,61). These studies pointed to several key phylogenetic groups as actively responding to the blooms and utilizing organic matter derived from phytoplankton. Bacteroidetes and Alpha-and Gammaproteobacteria were reportedly important during the blooms. Their relative contributions to total bacterial abundance and its variability have been studied intensively by using fluorescence in situ hybridization (FISH). However, as abundance is determined by both growth and mortality, changes in bacterial abundance do not always indicate changes in growth. Mainly because of some methodological limitations, little is known about the relative contributions of these key groups to total bacterial production or its va...

Impact of marine biogeochemistry on the chemical mixing state and cloud forming ability of nascent sea spray aerosol

“…The initial seawater contained a natural assemblage of bacteria and the added cultures of Alteromonas spp. bacteria (Table 2) each contained less than 10% of the total number of bacteria already present in the mesocosm, similar to the proportion of Alteromonas to total heterotrophic bacteria found in a phytoplankton bloom in the North Pacific [Tada et al, 2011]. A final aliquot of ZoBell media, a culture of the heterotrophic bacterium Pseudoalteromonas atlantica (strain 19262), and a culture of Dunaliella tertiolecta (green algae) were added to the wave channel, bringing chl a concentrations up to 5.5 mg m À3 .…”

Microbial production and consumption of marine dissolved organic matter

“…(Bell et al 1974, Lau et al 2007, Moreira et al 2011, Tada et al 2011, Trabelsi & Rassoulzadegan 2011, Nelson & Carlson 2012, Sarmento & Gasol 2012, Gómez-Consarnau et al 2012. Testing a diverse suite of DOM sources prepared in various ways allowed for investigating response dynamics of individual bacterioplankton strains to DOM sources of distinct size, chemistry and origin.…”

“…Using fluorescence in-situ hybridization, Yan et al (2009) Increased abundance of OM60 cells has also been shown to co-occur with algal blooms (Eilers et al, 2001;Alonso-Sáez et al, 2007;Yan et al, 2009) and many studies demonstrate that diverse low abundance taxa bloom under increasing concentrations of organic nutrients Eilers et al, 2000;Romera-Castillo et al, 2011;Tada et al, 2011;Nelson and Carlson, 2012). These opportunistic taxa exhibit a "feast or famine" lifestyle (Nissen, 1987;Flärdh et al, 1992;Srinivasan and Kjelleberg, 1998) and are often referred to as copiotrophs (Lauro et al, 2009;Yooseph et al, 2010).…”

“…A significant amount of work has also been performed in order to examine the response of bacterioplankton communities to other sources of DOM, including specific compounds, particular chemical and size fractions, and in-situ phytoplankton blooms (e.g. , Rink et al 2007, Tada et al 2011, Rinta-Kanto et al 2011, Teeling et al 2012, Gómez-Consarnau et al 2012. While these studies provide strong evidence for the structuring of bacterioplankton communities through variations in DOM composition and highlight the importance of both syntrophic and antagonistic interactions in DOM consumption, their inherent complexity precludes the identification of specific interactions between a single taxa and DOM component without a priori knowledge of a component's lability.…”

“…Decades of research by marine organic geochemists have revealed a wealth of information regarding the age and chemical characteristics of marine DOM; however, the identity and lability of individual DOM constituents remain largely unknown despite improvements in isolation and analytical technologies (Druffel et al 1992, Benner et al 1992, also reviews by Mopper et al 2007, Nebbioso & Piccolo 2012. Marine microbiologists have been measuring rates of microbial production (both primary and secondary) and respiration for decades (Baines & Pace 1991, Williams & Purdie 1991, also reviews by Duarte et al 2013, Williams et al 2013) and have recently begun using molecular approaches to examine DOM effects on microbial community structure and activity (Poretsky et al 2010, Vila-Costa et al 2010, Tada et al 2011, Trabelsi & Rassoulzadegan 2011, Mou et al 2011, Rinta-Kanto et al 2011, Romera-Castillo et al 2011, Nelson & Carlson 2012, Teeling et al 2012, Sarmento & Gasol 2012, Gómez-Consarnau et al 2012. These recent studies are revealing connections between various DOM sources and consumption by individual taxa, however it is not yet clear why these observed connections occur and the production of specific compounds by one microorganism has not yet been linked to their consumption by another.…”